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The mechanism of the evolutionary rate hypothesis

The mechanism of the evolutionary rate hypothesis


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There are several hypotheses for explaining the latitudinal gradients in species diversity (link). Of which, the evolutionary rate hypothesis states that warm temperature increases the rate of speciation. I want to know why warm temperature facilitates evolution.

This is not a question, but… some other hypotheses specifically discuss how a factor influences the rate of evolution (e.g., the size hypothesis discusses how large area can promote speciation). I think temperature hypothesis is a better name for the evolutionary rate hypothesis.


The mechanism of the evolutionary rate hypothesis - Biology

Evolution: Concepts and Mechanism

Introduction
Evolution is &ldquodescent with modification&rdquo (Charles Darwin). The questions evolution tries to address include: why are so many types of species on our plant? Where did they come from? How is it that they all appear to be so different but in fact are all somewhat related? The study on evolution has a tremendous impact on your life. For example, it can explain why doctors do or do not give antibiotics when you are sick, it can also explain the HIV world crisis.

Theory of Evolution
Theory of Evolution was first described by Charles Darwin. To understand &ldquodescent with modification&rdquo, one needs to understand 1) the idea that current day organisms arose from older ancestral species over time 2) Modification is a mechanism or process of interaction between the environment and an organisms to select for inheritable traits. Natural selection is one important mechanism of modification. If a species survives long enough, it has been selected naturally. The survival depends on an organisms fit to the environment. In another word, the organism best fit to the environment survive to propagate&mdashthis is called &ldquosurvival of the fittest&rdquo.

Origin of species
New species originate in the process of evolution. Speciation event occurs when members of a new reproductive community no longer interbreed with their ancestral population as a result of isolation and subsequent accumulation of adaptations to their new environment. Evolution includes multiple speciation events over time, which can be depicted with a phylogenetic tree. A phylogenetic tree shows a relationship between ancestor and descendant, i.e., the pattern of evolution. Most often the pattern is branching each branch containing the oldest ancestor in that line plus all of its descendants.

Scientific Steps to Darwin&rsquos Theory
Observation: 1) struggle of existence -- Reproducing organisms will produce more offspring than the environment can support if all offspring survive to reproduce 2) within any given population, there is a range of individual, heritable characteristics 3) survival depends on an organism&rsquos inherited traits. Hypothesis: 1) Attributes that lead to a better fit to an environment lead to greater chance for leaving behind offspring 2) Disproportionate reproductive success among population members lead to gradual change in traits of that population. Hypothesis Testing: 1) fossil record 2) comparative anatomy and embryology 3) Independent traits 4) DNA similarity.

Evolutionary Theory Today
Darwin thought evolution is a gradual process, today&rsquos evidence suggest that 1) evolution may follow a spurt and plateau pattern (punctuated equilibrium) 2) Changes of ecosystem play bigger roles in stimulating accumulation of new species then once thought 3) other mechanisms of species modification have been discovered such as gene flow and non-random mating, although natural selection remains the major player.

  • Stick-note type of explanation for easy understanding
  • Flowchart to show the process of natural selection
  • Example of a phylogenetic tree to show evolutionary relationship of monkeys and humans
  • Step-by-step deduction of Theory of Evolution
  • Why evolution is important?
  • Questions evolution tries to address
  • What is evolution?

Understanding Darwin&rsquos Theory of evolution

Scientific Steps to Darwin&rsquos Theory

  • Observations
  • Hypothesis
  • Hypothesis testing: evidence
  • Fossil record
  • Taxonomic groups
  • Independent Traits
  • Modern genetics
  • Gradualism vs. Punctuated Equilibrium
  • Global ecosystem change and evolution
  • Other mechanism of species evolution

See all 24 lessons in College Biology, including concept tutorials, problem drills and cheat sheets:
Teach Yourself College Biology Visually in 24 Hours


The COVID-19 Pandemic: A Lesson in Evolution, Biology, and Society (Evolution, Biology, and Society)

As the COVID-19 pandemic continues its devastating march around the globe and across the United States, only those who dismiss statistics about its deadly toll or denigrate the pain of those afflicted can ignore the handwriting on the chalkboard: We ignore at our peril the biological foundations of our being and the evolutionary processes that have shaped and continue to change our natural and social worlds. From the functioning of our social institutions to the consequences of our social divisions, nothing about us stands apart from nature. It is far from the first time that a pandemic has shattered social conventions and changed the course of social history, but the conjunction of the worldwide scope of COVID-19 with modern scientific tools for its investigation creates a better opportunity for learning the lesson a pandemic has to teach. The course of our society will depend on our ability to pass the test.

The earlier chapters in the historical textbook are no less compelling, but they could not offer at the time they were written the lesson we can learn today. When one-third of Europe’s population died excruciating and public deaths during the 14 th century plague, the pain experienced by families and communities was no less, but the confused response of barefoot penitents whipping themselves in public processions only exacerbated the threat (Tuchman 1978). When Christopher Columbus’s expedition and others initiated a pandemic that claimed the lives of 90 percent of indigenous Americans, it took more than 500 years for researchers to learn the lesson of what had actually happened (Mann 2011). By the time of the 1918 Spanish flu, Charles Darwin’s theory of evolution of species and modern biology allowed basic understanding of the viral threat, but events that facilitated the virus’s spread like Philadelphia’s massive celebration promoting war bonds demonstrated insufficient recognition of the implications for social policy. It is only in the last 30 years that evolutionary biologists and sociologists have demonstrated that survival of our species depended not only on our capacity to detect environmental or social threats but also on our ability to respond with highly coordinated, cooperative action: a template for effective response in the face of a pandemic (Wilson 2015).

Humans have evolved as a social species with a cognitive capacity for garnering feelings of safety and security from other individuals, a so-called ‘coalitional index’ (Boyer, Firat, & van Leeuwen, 2015). When historical conditions create inegalitarian societies based on social characteristics like race, ethnicity, sexualities, disabilities, these characteristics become perceptual cues triggering the formation of coalitional alliances and rivals, which create a bigger threat to our communities. But the exact evolutionary mechanisms that trigger group divides also serve as the infrastructure for human prosociality and altruism. Categorization based on perceptual cues like race is not inevitable (Kurzban, Tooby, & Cosmides, 2001) the concept of race itself belies the fact of the unity of the human species. And more importantly, when people form alliances across racial/ethnic boundaries, their well-being improves (Firat and Boyer, 2015), creating resilient communities that can bounce back in the face of calamities.

We only became who we are as a species because of our ability to support each other (Christakis 2019) we will “be swept away by the gale of history” if we forget this fundamental foundation for our well-being (Cohen 2020, Schutt 2020). COVID-19 is not the last pandemic humans will confront, nor the worst disaster our species has experienced in the past or can anticipate in the future (Schutt 2010). Our very survival depends on our ability to learn from the past, plan for the future, and use not just our evolved brains but our unique social abilities (Schutt, Seidman, & Keshavan 2015).


  • Mechanism of evolution is proposed by various theories and in that Landmark ′ s theory of “Inheritance of acquired characters” , De Vries ′ Mutation theory and Evolutionary by Natural selection (Darwinism) .
  • Darwin՚s theory of Natural selection still holds ground but was modified with progress in genetics and developed into the Modern synthetic theory which is regarded as the most valid theory of evolution.

Darwin՚s Theory of Natural Selection

  • Natural selection is a process in which individuals that are well suited to their environment will survive and reproduce better than their individuals.
  • Charles Darwin suggested that all kind of organisms are related through ancestry and a mechanism for evolution and named it natural selection. According Darwin, organisms produce more offspring than can survive because environmental resources are limited ant there ensues struggle for existence. Organisms with advantageous variations are protected and allowed to reproduce while the disadvantageous variants are limited from nature. This is the termed of natural selection by Darwin.
  • According to Darwin when the environment changes, new adaptations get selected in nature and after many generations sufficient characteristics will have been changed so as to alter the species into a new one (origin of species) .
  • Darwin talked about variation but did not know about the sources of variation. With progress in genetics the sources of variation were discovered, and Darwin՚s original theory of Natural Selection modified. This new theory was termed Neo-Darwinism or Modern Synthetic Theory.
  • The unit of evolution is population which has its own gene pool. Gene pool is the group of all different genes of a population.
  • Heritable genetic changes appear in the individuals of a population. These heritable changes or variations occur due to small mutations in the genes or in the chromosomes and their recombination՚s
  • Natural selection selects the variation which helps in adapting to the environment.
  • A change in the genetic constitution of a population selected by natural selection is responsible for evolution of a new species, since through interaction of variation and Natural Selection more offspring՚s with favorable genetic changes are born. This is called differential reproduction.
  • Once evolved, Reproductive Isolation helps in keeping species distinct.

Salient Features of Darwin՚S Theory of Natural Selection

  • Over production (Rapid Multiplication)
  • Limited Food and Space
  • Struggle for Existence
  • Appearance of Variations
  • Natural Selection or Survival of the Fittest
  • Inheritance of useful variations
  • Speciation (Formation of new species)
  • Get More on NIOS Senior Secondary Notes

What Can we Conclude from the Above Graph:

  • Increase in Relative EL exhibits a well defined pattern over the last 200 million years
  • Fastest growth was from 600--250 million years ago when species first emerged on the land
  • Mass extinctions clearly are important as they substantially alter the rate of growth
  • Unaltered rate would have produced current human level of EL about 60 million years ago
  • Continental rate is much higher than the oceanic rate
  • Smooth extrapolation backwards from last few million years of continental data suggests it takes 20 billion years for intelligence to emerge

It seems likely than when terrestrial ecosystems developed, the flow of nutrients to the oceans became impaired which served to suppress that ecosystems growth rate over the rest of geologic time.


3.4: Evolution theory’s core concepts

  • Contributed by Michael W. Klymkowsky and Melanie M. Cooper
  • Professors (MSCD and Chemistry) at University of Colorado Boulder and Michigan State University

So what are the facts and inferences upon which the Theory of Evolution is based? Two of its foundational observations are deeply interrelated and based on empirical observations associated with plant and animal breeding and the charateristics of natural populations. The first is the fact that whatever type of organism we examine, if we look carefully enough, making accurate measurements of visible and behavioral traits (this description of the organism is known as its phenotype), we find that individuals vary with respect to one another. More to the point, plant and animal breeders recognized that the offspring of controlled matings between individuals often displayed phenotypes similar to those of their parents, indicating that phenotypic traits can be inherited. Over many generations, domestic animal and plant breeders used what is now known as artificial selection to generate the range of domesticated plants and animals with highly exaggerated phenotypes. For example, beginning

10,000 years ago plant breeders in Mesoamerica developed modern corn (maize) by the selective breeding of variants of the grass teosinte. 68 All of the various breeds of dogs, from the tiny to the rather gigantic, appear to be derived from a common ancestor that lived between

19,000 to 32,000 years ago (although as always, be skeptical it could be that exactly where and when this common ancestor lived could be revised). 69 In all cases, the crafting of specific domesticated organisms followed the same pattern.

Organisms with desirable (or desired) traits were selected for breeding with one another. Organisms that did not have these traits were discarded and not permitted to breed. This process, carried out over hundreds to thousands of generations, led to organisms that display distinct or exaggerated forms of the selected trait. What is crucial to understand is that this strategy could work only if different versions of the trait were present in the original selected population and at least a part of this phenotypic variation was due to genetic, that is heritable, factors. Originally, what these heritable factors were was completely unclear, but we can refer to them as the organism&rsquos genotype, even though early plant and animal breeders would never have used that term.

This implies that different organisms have different genotypes and that different genotypes produce different phenotypes, but where genotypic differences came from was completely unclear to early plant and animal breeders. Were they imprinted on the organism in some way based on its experiences or were they the result of environmental factors? Was the genotype stable or could it be modified by experience? How were genotypic factors passed from generation to generation? And how, exactly, did a particular genotype produce or influence a specific phenotypic trait. As we will see, at least superficially, this last question still remains poorly resolved for many phenotypes.


Explaining differences in rates of evolution

The rate at which evolution produces new species of plants and animals, or at which existing species die out, is a subject of much interest -- and not only to scientists. That's because the rates of speciation and extinction can tell us much about the history of our planet. If lots of new species emerge during an interval, this would indicate favourable conditions for life on earth. In contrast, extraordinary events can trigger mass extinctions, the most famous example of which was the event that wiped out the dinosaurs 66 million years ago, probably caused by a meteorite impact.

Mysterious discrepancy

It is difficult to determine the frequency with which species in the past emerged and then went extinct again. "There was no one there to witness these processes as they occurred," says Rachel Warnock, a postdoc in the Computational Evolution research group at ETH Zurich. This is why scientists attempt to deduce the rates of speciation and extinction through indirect methods. Some information comes from fossils dated to different geological eras.

Another source of information comes from species that exist today. In particular, from what are known as phylogenetic (or evolutionary) trees of living species, which are based on DNA analysis. By applying statistical methods to these trees, scientists can determine how often new species emerged and old ones died off in the past.

However, these two approaches are problematic in that they often produce conflicting results: the speciation and extinction rates derived from the fossil record are often much higher than those calculated through phylogenetic methods. To date, it has been unclear what was responsible for this discrepancy.

Combining different approaches

But now, in collaboration with other scientists, Rachel Warnock and head of the Computational Evolution research group Tanja Stadler have found an explanation. "The two methods are based on different assumptions about how new species are formed," Warnock says. This is why they arrive at different conclusions. But if they account for these different assumptions, then it is possible to harmonise the results.

The researchers were able to demonstrate this by looking at various groups of animals, such as whales, canines and bovines. Their success was due in part to a computer model they developed themselves: "Now we're able to unify both perspectives," says Warnock. The results of their work were published in the journal Nature Communications.

Insights into speciation

Current thinking maintains that there is not one, but rather multiple mechanisms by which new species emerge (see box). Each mechanism leads to different results the process may produce one or two new species, while the original species either continues to exist or dies out. "When using the statistical methods to analyse phylogenies and fossils, scientists have thus far not taken these different possibilities explicitly into account," Warnock says.

The new model now incorporates them, thus ensuring that fossil-based and phylogenetic information produce compatible speciation and extinction rates.

It also provides indications as to which speciation mechanism predominated in a particular animal or plant group. For example, the evolutionary tree and the fossil record of whales reveals that the most frequent mode may be anagenesis that is, original species are gradually transformed into new ones (mode 3 see box). In consequence, the model could be used in future studies to gain new insights into the evolution of organisms. It also helps to harmonise the results of fossil based and phylogenetic analysis better than before.

Three ways in which new species can emerge:

  • Budding: A new species branches off from an existing one, which continues to exist (1 new, 0 extinct).
  • Cladogenesis: A species splits into two new species, with the ancestral form dying out (2 new, 1 extinct).
  • Anagenesis: A species develops further into a new species, with the ancestral form dying out in the process (1 new, 1 extinct).

Starting with a single species, new species may emerge in any of the three ways. In their study, ETH researchers examined whether certain species gave rise to new ones in one predominant way.


Biology Homework Chapter 13: Evolution - Natural Selection

Textbook assignment: Chapter 13: How Populations Evolove, sections 1-11.

Study Notes
  • 13.1 The text presents evolution as the central theory of biology, the thread that ties all the other pieces together. Keep this in mind as we study this unit and the next, both of which address the similarities between organisms (based on the common chemical processes and cell functions we have been studying) and the differences that exist between species and between individuals.
  • 13.2 Fossil evidence is used to try to establish a sequence of development based on geological interpretation of the age of the rocks containing the fossils. Dating is done by comparing levels of radioactive isotopes (we have to make assumptions about the starting concentrations of the isotopes), and by looking at stratification levels.
  • 13.3 Fossils of transitional forms of specific species appear to support the hypothesis that adaptations for new functions occurred.
  • 13.4-5 Common structures (homologous structures) with different functions are used to supplement fossils as evidence for evolution. The inheritance of common structures can be traced as well through molecular biology (DNA sequence studies). In some species, homologous structures appear in the embryo but not in adult individuals. These patterns can be used to map how similar different species are. The greater the DNA sequence similarity is, the more recently the species diverged.
  • 13.6 Darwin proposed natural selection as a mechanism to explain changes in the distribution of characteristics in individuals of a species over time. In this part of his theory, no new species are created, but the frequency of a given trait in a population shifts over time as those members of a species who lack the form of critical traits that allow them to survive fail to reproduce.
  • 13.7 Natural selection occurs in modern populations and can be observed even over short periods of time. One example is the development of resistant strains of insects following widespread use of insecticides.
  • 13.8 The only factors that can introduce new traits are mutations in the nucleotide sequences of DNA. "Learned traits" cannot be passed on through any material means. New combinations of traits occur naturally when sexual reproduction includes the mechanism of "crossing-over" during meiosis.
  • 13.9 Evolution is not used to explain changes in an individual, but in traits expressed in populations. The only traits that can be considered must be inheritable traits. Over time, the fraction of a population's individuals carrying a particular trait (allele for a given gene) will change in response to environmental factors.
  • 13.10 The Hardy-Weinberg equation predicts the percentage of a population with a given trait if NO environmental factors influence it. Changes in the population indicate the level of environmental factors acting on the population. Equilibrium requires calculation of the Hardy-Weinberg equation in large populations with no mutation, random mating, and on external influences.
  • 13.11 Public health organizations use the Hardy-Weinberg principles to determine whether non-random changes are occurring in the population.

Web Lecture

Read the following weblecture before chat: The theory of evolution

Take notes on any questions you have, and be prepared to discuss the lecture in chat.

Perform the study activity below:

Check out the Evolution in Action game at the PBS Nova site. Click on Launch interactive. Read the Rules and Instructions (available from buttons in the lower right of the game screen). How does changing the environment (changing the background colors) change the population?

Chat Preparation Activities

  • Essay question: The Moodle forum for the session will assign a specific study question for you to prepare for chat. You need to read this question and post your answer before chat starts for this session.
  • Mastery Exercise: The Moodle Mastery exercise for the chapter will contain sections related to our chat topic. Try to complete these before the chat starts, so that you can ask questions.

Chapter Quiz

Lab Work

© 2005 - 2021 This course is offered through Scholars Online, a non-profit organization supporting classical Christian education through online courses. Permission to copy course content (lessons and labs) for personal study is granted to students currently or formerly enrolled in the course through Scholars Online. Reproduction for any other purpose, without the express written consent of the author, is prohibited.


Evolution of C4 plants: a new hypothesis for an interaction of CO2 and water relations mediated by plant hydraulics

C4 photosynthesis has evolved more than 60 times as a carbon-concentrating mechanism to augment the ancestral C3 photosynthetic pathway. The rate and the efficiency of photosynthesis are greater in the C4 than C3 type under atmospheric CO2 depletion, high light and temperature, suggesting these factors as important selective agents. This hypothesis is consistent with comparative analyses of grasses, which indicate repeated evolutionary transitions from shaded forest to open habitats. However, such environmental transitions also impact strongly on plant–water relations. We hypothesize that excessive demand for water transport associated with low CO2, high light and temperature would have selected for C4 photosynthesis not only to increase the efficiency and rate of photosynthesis, but also as a water-conserving mechanism. Our proposal is supported by evidence from the literature and physiological models. The C4 pathway allows high rates of photosynthesis at low stomatal conductance, even given low atmospheric CO2. The resultant decrease in transpiration protects the hydraulic system, allowing stomata to remain open and photosynthesis to be sustained for longer under drying atmospheric and soil conditions. The evolution of C4 photosynthesis therefore simultaneously improved plant carbon and water relations, conferring strong benefits as atmospheric CO2 declined and ecological demand for water rose.

1. Photosynthetic conservatism and diversity

Photosynthesis has evolved only once, and every photoautotrophic organism on Earth uses the same ‘C3 pathway’ [1]. This biochemical cycle employs the enzyme Rubisco to fix CO2 into a five-carbon acceptor molecule, producing three-carbon organic acids, upon which ATP and NADPH produced from the light reactions are deployed to generate sugars and to regenerate the acceptor molecule. The pigments and proteins involved in C3 photosynthesis are highly conserved across photosynthetic organisms, and this pathway operates unmodified in the majority of species, termed ‘C3 plants’. However, the basic C3 pathway has also been augmented by carbon-concentrating mechanisms (CCMs) in multiple lineages, many of which evolved during the Early Neogene following a massive depletion of atmospheric CO2 [2–5].

‘C4 photosynthesis’ is a collective term for CCMs which initially fix carbon into four-carbon organic acids via the enzyme phosphoenolpyruvate carboxylase (PEPC) [6], and then liberate CO2 from these C4 acids to feed the C3 pathway within a compartment of the cell or leaf [7,8] (figure 1a). The compartment is isolated from the atmosphere and resists CO2-leakage, so that CO2 is enriched at the active site of Rubisco [12] (figure 1a). Coordination of C4 and C3 biochemical pathways requires complex changes to metabolism, and the compartmentation of these pathways usually relies on a specialized leaf anatomy (figure 1b). C4 photosynthesis is therefore a complex trait based on the transcriptional regulation of hundreds of genes [13], coupled with post-transcriptional regulation [14] and the adaptation of protein-coding sequences [15].

Figure 1. Mechanism of C4 photosynthesis. (a) Simplified schematic of the C4 syndrome, showing how the C3 pathway is isolated from the atmosphere in most C4 species within a specialized tissue composed of bundle sheath cells (BSC). The C4 pathway captures CO2 within mesophyll cells (MC) using the enzymes carbonic anyhdrase (CA) and phosphoenolpyruvate carboxylase (PEPC). It then transports fixed carbon to the BSC where decarboxylase enzymes (DC) liberate CO2, which accumulates to high concentrations around Rubisco. (b) Transverse section of a C4 leaf, showing the arrangement of MC and BSC. In this picture, the BSC are thicker walled, are stained darker and form rings surrounding the veins (adapted from Watson & Dallwitz [9]). Enlarged BSC relative to MC and close vein spacing are typical of C4 leaves, and this pattern is referred to as ‘Kranz anatomy’. (c) Explanation of how variation in CO2 and temperature favours C3 or C4 species [10,11]. The schematic shows the range of CO2 partial pressures and temperatures predicted to favour the growth of either C3 or C4 species, based on the maximum quantum yield of photosynthesis. Quantum yield is a measure of photosynthetic efficiency, which declines in C3 plants as photorespiration increases at low CO2 and high temperature, (reproduced with permission from Edwards et al. [3], which was adapted from Ehleringer et al. [11]).

Despite the complexity of C4 photosynthesis, it has been recorded in more than 60 plant lineages [16]. This striking evolutionary convergence probably arises because the pathway is constructed from numerous pre-existing gene networks [17], and altered levels and patterns of expression of enzymes that are already present in C3 leaves [18–20]. Many of the known C4 lineages occur in clusters, suggesting that they share early steps on the evolutionary trajectory towards C4 photosynthesis, taking an independent path only during later stages of the process [21].

In recent years, evidence from genomics, molecular genetics, physiology, ecology, biogeography, evolutionary biology and geosciences has enriched our understanding of when, where and how C4 photosynthesis evolved. Here, we extend previous work that focused on why the pathway evolved, based on the environmental conditions that drove natural selection. We begin by reviewing the well-established current hypothesis that atmospheric CO2 depletion, high temperatures and open environments selected for the C4 pathway as a means of directly improving photosynthetic rate and efficiency. Our main objective is to introduce a new dimension to these ideas, by proposing that these same environmental conditions—CO2 depletion, high temperatures and open environments—as well as seasonal drought, would also select for C4 photosynthesis for an additional reason i.e. to compensate for the strain on the plant hydraulic system resulting from excessive demand for water transport. Our hypothesis is consistent with recent comparative analyses of ecological niche evolution and plant physiology, which suggest important effects of the C4 pathway on plant–water relations. We support our proposal with evidence from the literature, and mechanistic models that integrate the latest understanding of how hydraulics, stomata and photosynthesis are coordinated within leaves. Our central focus is on grasses, but we complement our analysis with additional evidence from eudicots.

2. Environmental selection on photosynthetic efficiency

Atmospheric CO2 depletion has long been advocated as the primary selection pressure for C4 CCMs, through its differential effects on the efficiency of C3 and C4 photosynthesis [22]. This difference arises because the active site of Rubisco is unable to discriminate completely between CO2 and O2, and catalyses the fixation of both molecules [23,24]. The oxygenation reaction generates toxic intermediates that must be metabolized via photorespiration to render them harmless and to recover carbon. Oxygenation renders photosynthesis less efficient because it competes directly with carboxylation (CO2-fixation), and because photorespiration consumes the products of photochemistry and liberates CO2. In a C3 plant, the ratio of carboxylation to oxygenation (and therefore photosynthetic efficiency) decreases rapidly with declining atmospheric CO2, especially at high temperatures [25]. In contrast, by fixing the bicarbonate ion rather than CO2, the C4 pathway does not confuse CO2 with O2 (figure 1a). Furthermore, by isolating Rubisco from the atmosphere and concentrating CO2 at its active site [26], it also minimizes oxygenation in the C3 pathway. However, energy required to run the C4 CCM imposes a cost on photosynthetic efficiency under all conditions [27,28]. This means that the efficiency of C4 photosynthesis is only greater than the C3 type under conditions that promote high rates of photorespiration [19]. Low atmospheric CO2 and high temperatures are considered especially important in favouring C4 photosynthesis, with a ‘crossover threshold’ for CO2 of 35–55 Pa and temperatures of 25–30°C (figure 1c [10,11]).

A further physiological difference between C3 and C4 species arises because the carboxylation reaction of Rubisco is strongly limited by its substrate when CO2 falls below approximately 70 Pa at the active site [29]. Resistances to CO2 diffusion from the atmosphere to the chloroplast mean that this limitation arises when atmospheric CO2 levels fall below approximately 100 Pa. In contrast, significant CO2-limitation only occurs in C4 plants at atmospheric CO2 levels of less than 20 Pa [30]. The CO2-saturation of Rubisco in C4 photosynthesis means that in high light environments the enzyme reaches its saturated catalytic rate, maximizing the photosynthetic difference between C3 and C4 species. As a consequence, in open habitats, the ‘crossover threshold’ is raised to higher CO2 concentrations and lower temperatures [31]. Conversely, the cool shade of forest understorey environments offers little benefit for the C4 pathway over the C3 type [32], although once C4 evolves in a lineage, descendent species may invade shaded habitats by modifying their tissue costs, allowing them to maintain an advantage in photosynthetic rate over co-occurring C3 species [33].

Water relations have previously been proposed to influence the evolution of C4 photosynthesis in an indirect way. For terrestrial vascular plants, the loss of water is an inevitable cost of photosynthesis, regulated by turgor-mediated decreases in the aperture of stomatal pores. The partial closure of stomata to conserve water in arid and saline soils or dry atmospheric conditions (characterized by high vapour pressure deficit (VPD)) has been hypothesized to select for the C4 pathway via indirect effects on photosynthetic efficiency [34]. Thus, reduced stomatal aperture (i) restricts the CO2 supply to photosynthesis and (ii) decreases transpiration, thereby reducing latent heat loss and raising leaf temperature. Both effects increase photorespiration, depressing the efficiency of C3 photosynthesis, and favouring the C4 type.

Therefore, the general expectation based on physiological evidence is that declining atmospheric CO2 should select for C4 photosynthesis in hot, open and dry or saline environments, where photorespiration is especially high in C3 species [19].

3. Ecological drivers of c4 pathway evolution

Recent data on the timing of C4 origins and geological history have supported these ideas for the importance of low CO2 and high temperature and irradiance, but also highlight the importance of aridity. First, the modelling of evolutionary transitions from C3 to C4 photosynthesis using time-calibrated molecular phylogenies indicated that C4 origins have all occurred over the past 30 Myr, with no difference in timing between monocot and eudicot lineages (figure 2) [35–37]. Secondly, multiple geological proxies suggested that atmospheric CO2 has remained below 60 Pa for most of this 30 Myr interval (figure 2), after a dramatic decline during the Oligocene (23–34 Ma) that corresponds to the onset of Antarctic glaciation [4]. Therefore, C4 photosynthesis does seem to have evolved in a CO2-depleted atmosphere, within the ranges of uncertainty that are inherent to phylogenetic and geological evidence [4,37].

Figure 2. Geological history of atmospheric CO2 and the estimated ages of C4 evolutionary origins. The palaeo-atmospheric CO2 history of the Cenozoic is reconstructed from multiple independent proxies (pale grey circles), with a smoothed line of best fit encompassing all of the evidence (reproduced with permission from Beerling & Royer [4]). The estimated ages of C4 evolutionary origins in grasses (dark grey horizontal bars) and eudicots (black horizontal bars) were obtained using phylogenetic inference and calibration to fossils [35]. Thick bars represent uncertainty in the position of each C4 evolutionary origin on the phylogeny, while thin bars indicate uncertainty in dating of the phylogeny (reproduced with permission from Christin et al. [35]).

The hypothesis that high temperatures select for C4 photosynthesis has been supported for 30 years by invoking the observation that species richness of C4 grasses increases along latitudinal and altitudinal temperature gradients [32,38,39]. However, phylogenetic comparative analyses have shown that C4 species do not live in warmer environments than their closest C3 relatives. First, Edwards & Still [40] showed that the absence of C4 species from high altitudes in the predominantly exotic grass flora of Hawaii [39] is better explained by phylogenetic history than photosynthetic pathway. The exclusively C3 lineage Pooideae is most speciose at cool, high elevations. However, species of the PACMAD lineage are most numerous in the warm lowlands, irrespective of whether they use C3 or C4 photosynthesis. Edwards & Smith [41] further investigated this pattern by reconstructing the evolution of temperature niche in the world's grasses. Their analysis indicated that grasses originated in the tropics. The C3 and C4 species of the PACMAD clade have remained predominantly in these warm environments, irrespective of photosynthetic pathway, while Pooideae have adapted to and radiated in low-temperature environments. Thus, C4 photosynthesis did evolve at high temperatures, but the major innovation that caused ecological sorting of grasses along temperature gradients was the adaptation of certain C3 lineages to cold conditions [41].

Comparative analyses also support the hypothesis that the C4 pathway in grasses evolved in open environments. First, by modelling the rate of evolutionary transitions between C3 and C4 photosynthesis, and shaded and open habitats, Osborne & Freckleton [42] showed that C4 origins were significantly more likely to have occurred in open than shaded environments. Secondly, Edwards & Smith [41] quantified the shift in environmental niche that is correlated with evolutionary transitions from C3 to C4 photosynthesis. The origins of C4 photosynthesis were generally associated with migration from an aseasonal tropical niche into a seasonal, sub-tropical one, an ecological shift consistent with a transition from moist tropical forest to drier, more open woodland or savannah habitats [41]. These complementary analyses suggest that C4 photosynthesis evolved in C3 species that had migrated out of their ancestral niche in tropical forests, and invaded open sub-tropical woodland or savannah habitats. The C4 pathway, therefore, seems to be a key adaptation to one of the most important ecological transitions in the evolutionary history of grasses [43], which ultimately enabled the assembly of the tropical grassland biome.

The proportion of C4 species in eudicot floras increases along gradients of rising aridity [11]. Recent comparative analyses at the regional and global scales show that, in addition to preferring open habitats, C4 grasses have also sorted into drier environmental niches than their C3 relatives [40–42]. However, for grasses, there is no evidence that C4 photosynthesis is more likely to evolve in xeric than mesic habitats [42]. Rather, the distribution of C4 species in dry areas can be explained by two inferences from comparative analyses: (i) that C4 origins were accompanied by shifts to a drier ecological niche within the humid sub-tropics [41] and (ii) a greater likelihood that C4 than C3 lineages will invade very dry (xeric) environments [42]. In some systems, C4 grasses tolerate greater aridity than C3 species of adjacent areas for example, it has been argued that certain C4 grasses of the Kalahari occur in areas too dry for the C3 type to persist [44]. Water relations clearly play an important role in the ecology and biogeography of both C4 monocots and C4 eudicots.

A corpus of physiological work and comparative analyses therefore supports the theory of how low atmospheric CO2 drove selection for improved photosynthetic rate and efficiency in hot and open environments over the last 30 Myr. What has been missing is an understanding of the importance of plant–water relations in differentiating photosynthetic types in such environments.

4. Strain on plant–water relations in a co2-depleted atmosphere

Multiple strands of geological, ecological and physiological evidence indicate that a restriction in water supply and an increase in evaporative demand were important ecological factors during the evolution of C4 species. First, permanent ice sheets of low CO2 ‘icehouse’ climate intervals are known to reduce atmospheric moisture levels, with cool temperatures reducing the intensity of the hydrological cycle and increasing climatic seasonality [45]. As a consequence, the CO2-depleted ‘icehouse’ climate of the last 30 Myr has caused the ecological availability of water to decline across large parts of the Earth's surface.

Paleontological evidence reveals that open woodland, savannah and grassland vegetation had begun to extend over large areas of the tropics and subtropics by the Miocene (24–6 Ma) [3,46]. By analogy with processes in the modern world, these open tropical and sub-tropical ecosystems are likely to have been generated by seasonal aridity, edaphic conditions that exclude trees (including high salinity), and disturbance by fire and large mammalian herbivores [3,47–49]. Low atmospheric CO2 may interact with each of these processes by limiting tree growth [50–52]. In fire-prone environments, this limitation means that trees are less likely to become large enough to survive surface fires [51,53]. Indeed, in contemporary mesic savannahs, woody plant cover is apparently increasing in response to rising CO2 [53]. C4 plants are generally short-statured herbs, and only trees in exceptionally rare cases (several species of Hawaiian C4Euphorbia are fully trees, including rainforest as well as dry forest species and Haloxylon trees of West Asia have C4 photosynthetic stems). The central role of seasonal aridity in reducing forest cover therefore means that the early C4 plants living in open tropical and sub-tropical environments may well have been subjected to fire events and/or episodes of soil drying.

The demand for water imposed by potential evapotranspiration (PET) is also significantly greater for plants in open habitats than in shaded understorey environments. This environmental contrast is caused by a suite of interrelated microclimatic effects associated with tree cover, illustrated in figure 3 using field observations and a model of leaf energy balance and evaporation (appendix A). Micrometeorological data are shown in figure 3a,b for transects crossing a rainforest edge into adjacent pasture in tropical (Mexico) and temperate (New Zealand) localities [54,55]. Closed forest canopies typically intercept greater than 95 per cent of incident shortwave radiation (figure 3a,b). A model of leaf energy balance shows that this markedly reduces the net radiation and therefore the energy available to drive evaporation (latent heat flux) at ground level (figure 3c,d). Shading of the land surface under a forest canopy also causes a decrease in the air temperature at ground level (from 28 to 25°C in the tropical example, and from 10 to 5°C in the temperate example figure 3). Therefore, the vapour pressure gradient driving transpiration, as indicated by the VPD, also declines (figure 3a,b). Finally, windspeed is lower in forested compared with open environments (figure 3a,b). This reduces the leaf boundary layer conductance to water vapour (figure 3e,f) and further slows the modelled rate of evaporation. The overall effect of this micrometeorological gradient is a massive difference in the PET modelled for leaves in forested compared with open environments (figure 3e,f appendix A). In the examples illustrated in figure 3, modelled PET is close to zero in the humid forest understorey, but exceeds 10 mmol H2O m −2 s −1 in the adjacent open pasture for both tropical and temperate climates (figure 3e,f).

Figure 3. Micrometeorological gradient spanning the transition from forested to open habitats. Data are shown for (a,c,e) pasture at the edge of tropical rainforest and (b,d,f) temperate rainforest, plotted against distance into the forest (negative values for distance = pasture positive values = forest). Micrometeorological observations of photosynthetically active radiation (PAR), vapour pressure deficit (VPD) and surface windspeed are shown for (a) Mexico [54] and (b) New Zealand [55]. From these data, net radiation, latent and sensible heat fluxes are calculated using the model outlined in appendix A for the (c) tropical and (d) temperate forests. Calculated values of potential evapotranspiration (PET) and boundary layer conductance (ga) are also shown for the same (e) tropical and (f) temperate localities.

In fact, the risk of colonizing exposed habits depends on the actual rate of leaf transpiration (E), which is lower than PET, being determined by the coupling of micrometeorological effects with the leaf stomatal conductance to water vapour (gs). The gs is controlled by changes in stomatal aperture, which are regulated by leaf water status, photosynthetic rate and chemical signals reflecting the soil water status transmitted from roots to leaves [56]. The gs plays a pivotal role in leaf gas exchange, limiting both the efflux of water and influx of CO2, and the C4 CCM causes a large shift in this trade-off between carbon gain and water loss. For any given value of gs, the net rate of leaf photosynthetic CO2 uptake (A) is greater for C4 than C3 species. This contrast is illustrated in figure 4a for interspecific comparisons of closely related C3 and C4 PACMAD grass species. Measurements were made under modern atmospheric CO2 levels, and in high light and temperature conditions representative of a warm, open environment. The contrast is also modelled in figure 4b using models of leaf gas exchange for idealized C3 [59] and C4 [29] species (see appendix B). In the interspecific comparison, photosynthesis at 30°C can span the same range in C3 and C4 species, with one exceptionally high value of A in the C3 species exceeding the highest values observed in the C4 species (figure 4a [57]). However, high A for C3 species comes at enormous cost in terms of gs (figure 4a,b), and elevated rates of CO2-fixation are therefore achieved with far greater water economy in C4 than C3 leaves (i.e. with greater water-use efficiency (WUE), defined as A relative to E). The ecological significance of this difference is underscored by the fact that the exceptionally high C3 value of A in figure 4a was measured in the wetland species Phragmites australis, whereas the highest C4 value was in the savannah species Eriachne aristidea [57].

Figure 4. Illustration of the relationships of photosynthesis (A) to stomatal conductance (gs) in C3 and C4 species [57,58]. (a) Interspecific comparison of PACMAD grass species under high light and the current ambient CO2 level (filled symbols, C3 open symbols, C4 circles from Taylor et al. [58], photosynthetic photon flux density (PPFD) = 1300 µmol m −2 s −1 , temperature = approx. 25°C, VPD = 1 kPa triangles from Taylor et al. [57], PPFD = 2500 µmol m −2 s −1 , temperature = 30°C, VPD = 0.8–1.5 kPa). Fitting a general linear model to these data showed that the slope of A on gs was significantly steeper among C4 than C3 species (125 versus 29 µmol CO2 mol −1 H2O, respectively F1,42 = 55.8, p < 0.0001), with a significant quadratic term that shows no interaction with photosynthetic pathway. (b) Intraspecific response simulated for a C3 and a C4 species by prescribing variation in gs, and modelling A using the approach described in appendix B. Note the saturation response in C3 and linear response in C4, indicating the greater sensitivity of A to stomatal closure in C4, despite achieving higher maximum A at its maximum gs.

The greater WUE of C4 compared with C3 photosynthesis arises from both differences in stomatal aperture and the kinetic properties of the carboxylase enzymes employed by each pathway (figure 1a). PEPC in C4 plants is able to fix carbon at a much higher rate than Rubisco in C3 plants at in vivo substrate concentrations [29]. This allows the C4 pathway to generate a much steeper air–leaf CO2 gradient and higher rates of photosynthesis for a given value of gs. The lower E and greater WUE of C4 than C3 plants was first recognized more than 40 years ago [60], although it is subject to ecological adaptation that can lead to significant interspecific variation and thus overlaps in the ranges of photosynthesis and transpiration for the two photosynthetic types [61]. However, recent work sampling multiple independent lineages of C4 grasses from a range of different habitats showed that gs is significantly lower in each lineage of C4 species than in closely related lineages of C3 grasses [57,58].

The need for a lower gs to conserve water is especially strong when CO2 levels fall and leaves tend to open stomata to maintain photosynthesis. Data compiled from five independent experiments demonstrate that gs in both C3 and C4 plants increases dramatically in response to the depletion of atmospheric CO2 to sub-ambient levels (figure 5). This negative relationship of gs to CO2 is apparently independent of the responsiveness of gs to VPD [68], and partially or fully offsets the CO2-limitation of photosynthesis at the cost of greater water use. A general linear model fitted to ln-transformed data shows a significant effect of photosynthetic pathway on the intercept of this relationship of gs to CO2 depletion, supporting the generality of higher gs in C3 than C4 species (figure 5a). However, there is no difference in the slope of this relationship between C3 and C4 species (figure 5), indicating a similar relative increase in gs with declining atmospheric CO2 for C3 and C4 species. This finding is consistent with previous meta-analyses showing similar relative declines in gs with CO2 enrichment in C3 and C4 grasses [66,67]. Notably, because gs is typically higher in C3 than C4 species, a similar relative response to CO2 translates into a larger absolute effect (figure 5b). For example, for the model fitted in figure 5b, a depletion of atmospheric CO2 from 100 to 30 Pa equivalent to the Oligocene CO2 drop (figure 2) results in a rise in gs from 0.23 to 0.61 mol H2O m −2 s −1 in C3, but only from 0.08 to 0.21 mol H2O m −2 s −1 in C4 species.

Figure 5. Stomatal conductance (gs) for the leaves of C3 and C4 plants grown and measured under a range of different CO2 partial pressures, with an emphasis on experiments investigating the effects of CO2 below the current ambient level of approximately 40 Pa (data sources: [30,62–65] electronic supplementary material). The data compilation is based on literature searches for studies reporting the leaf gas exchange of plants under sub-ambient CO2. However, values for elevated CO2 were included when they were reported as part of the same CO2-gradient studies. The fitted curve for the C3 species is ln(gs) = 2.16 − 0.78 ln(CO2), and for the C4 is ln(gs) = 1.10 − 0.78 ln(CO2). Data and curves are shown on (a) log and (b) linear plots to illustrate relative and absolute sensitivity to CO2, respectively. The fitted curves produce effect sizes for gs at elevated CO2 in C3 and C4 grasses that fall within confidence intervals of previous meta-analyses [66,67]. Filled circles, C3 open circles, C4.

We explored the implications of these contrasting stomatal responses to CO2 in C3 and C4 leaves by modelling leaf transpiration and energy balance (appendix A). Simulations with the model made the simplifying assumption that stomata respond only directly to CO2, with no hydraulic or hormonal feedback on gs. We compared the modelled response of E to CO2 under four sets of micrometeorological conditions representing either an open pasture or a shaded rainforest understorey, in a humid tropical or temperate climate (using the data from figure 3). Our model simulations showed that falling atmospheric CO2 drove larger increases of gs and E in C3 than C4 species (figure 6a,b) this contrast was especially pronounced in open, tropical environments (figure 6a). For the simulations shown in figure 6a, we used a high relative humidity of 80 per cent (VPD = 0.6 kPa), which is typical of the moist tropics and the summer growing season in the humid subtropics (e.g. figure 3a). Under these conditions, simulated E in the C3 species exceeded 6 mmol H2O m −2 s −1 Mpa −1 at a CO2 level of less than 40 Pa (figure 6a). Assuming a leaf-specific whole- plant hydraulic conductance (Kplant) of 12 mmol H2O m −2 s −1 in grasses, and a 50 per cent decline in Kplant under a soil–leaf water potential gradient of −1 MPa [69], this transpiration rate would be sufficient to cause 50 per cent failure of the hydraulic system. The threshold was not reached in a C4 leaf under these conditions. In a drier atmosphere of 60 per cent relative humidity (VPD = 1.5 kPa), the threshold for 50 per cent hydraulic failure in the C3 leaf was reached at CO2 < 80 Pa, and in the C4 at < 20 Pa (data not shown). The contrast was yet more pronounced at a VPD of 3.0 kPa, which is typical of hot, arid climates. Here, 50 per cent hydraulic failure occurred for the C3 leaf at CO2 < 150 Pa, and for the C4 leaf at CO2 < 50 Pa (data not shown).

Figure 6. Modelled response of transpiration to CO2 for C3 and C4 leaves in open (solid lines) and shaded rainforest understorey (dashed lines) conditions in either (a) humid tropical or (b) humid temperate climates. The model is described in appendix A. Horizontal dashed lines indicate the transpiration rate that would cause 50% hydraulic failure in the absence of feedbacks on stomatal conductance. Filled circles, C3 open circles, C4.

Thus, to avoid failure of the vascular system in open, tropical environments, hydraulic regulation of stomata, investment in hydraulic supply, or a reduction in leaf area [62], would be required at a considerably higher atmospheric CO2 partial pressure in C3 than C4 species. Coupled with the inference that open tropical habitats selected for the C4 pathway in grasses, this observation points strongly to plant–water relations as a potential driver of C4 evolution.

5. Hypothesis for a central importance of hydraulics in c4 evolution

The current consensus model for the evolution of C4 photosynthesis has been developed over 25 years [19]. The evolutionary trajectory from C3 to C4 photosynthesis, via C3–C4 intermediates, is framed in terms of distinct phases for the sake of clarity however, in reality, these are likely to overlap, and certain developments may occur earlier or later in the sequence. A simplified model of the phases is outlined in table 1, and Sage [19] provides both a comprehensive review of the evidence underpinning this model and the detailed mechanisms proposed. As with the evolution of any complex trait, each step must provide a selective advantage over the previous phase or be selectively neutral.

Table 1. Hypothetical model for the evolution of C4 photosynthesis, showing three phases that are each observed in extant C3–C4 intermediates. The scheme is a simplified version of that presented by Sage [19], incorporating new evidence [70].

We propose that atmospheric CO2 depletion and open environments select indirectly for C4 photosynthesis via plant–water relations at two points during the evolutionary sequence (table 1, phases 1 and 3). This mechanism acts in combination with the well-established effects of atmospheric CO2 depletion and open environments on photorespiration. A direct role of water relations provides a clear explanation for many of the anatomical changes in the early evolution of C3–C4 intermediacy these are observed in other lineages of C3, C4 and CAM species, which indicates that these steps are not rare or extraordinary events, but that C4 evolution simply co-opts typical steps in adaptation to dry environments.

Evolution of ‘proto-Kranz anatomy’ (table 1, phase 1). Our hypothesized hydraulic mechanism is based on the vulnerability of C3 leaves to desiccation and hydraulic failure under conditions of high evaporative demand in hot, open environments. Indeed, as described above, the hydraulic vulnerability of leaves would have increased dramatically as C3 grass species migrated from the understorey of a tropical forest into more open tropical environments. If stomata close to protect the hydraulic system, the plant eventually faces carbon starvation through photorespiration and the depletion of carbon stores [73,74]. Carbon starvation is also exacerbated by atmospheric CO2 depletion [75]. These conditions would select for greater hydraulic capacity in C3 leaves, enabling greater gs to achieve rapid rates of photosynthesis in periods when water is abundant, and reducing both the requirement for stomatal closure and the risk of hydraulic failure as stomata partially close in a drying soil or under increasing VPD.

Notably, the anatomical preconditioning required for C4 is precisely that expected to evolve in C3 plants under selection for greater tolerance of dry soil, open environments, high VPD and/or low CO2. Previous studies of adaptation to these conditions within species or across closely related species within given lineages have shown increased vein densities, and thus shorter interveinal distances [76–79]. This higher vein density would permit greater gs and higher A during periods with high water availability, to compensate for low CO2. Indeed, the evolution of greater vein density in the early angiosperms may have allowed them to better cope with low CO2, while avoiding stomatal closure, contributing to or driving their contemporary dominance of world vegetation [78,80]. The higher vein densities in C4 than C3 species may indicate an extension of that trend, i.e. an adaptation to the water deficit that accompanies higher demand from transpiration to maintain photosynthetic rate in low CO2. In the same way that an increase in vein density may have enabled angiosperms to displace gymnosperms in dominating the world's forests, this trend in grasses may have provided a competitive advantage over grasses with lower vein densities, contributing to their dominance over large areas of the planet. The high vein densities in species with ‘proto-Kranz anatomy’ led to this feature being co-opted as an early part of the C4 syndrome, providing enough tissue to later serve as the locus of sequestered C3 metabolism (figure 1a,b) [19,71,72,81,82].

Similarly, the enlargement of bundle sheath during the early phase of C4 evolution may have contributed water storage capacitance to the tissue [19,71]. Indeed, the evolution of such tissue in species with ‘proto-Kranz anatomy’ would be an extension of a frequently observed trend in certain plant lineages in which the species adapted to saline and drier climates have more strongly developed achlorophyllous, large-celled tissue. This tissue serves an apparent function for water storage either in the bundle sheath, mesophyll or hypodermal layers, and this trend of greater water storage with aridity is apparent within C3 lineages with leaves [83,84] and phyllodes [85], but also within C4 and CAM lineages [86,87] (M. J. Sporck & L. Sack 2011, unpublished data).

Evolution of the C4cycle (table 1, phase 3). The evolution of greater WUE is apparently an important step in C4 evolution. It may be achieved in certain C3–C4 intermediates operating a photorespiratory pump (table 1, phase 2) through the enhancement of A for a given gs (e.g. Heliotropium [88]). However, once the carboxylase activity of PEPC exceeds that of Rubisco (evolution of ‘C4-like’ plants during phase 3, table 1), further improvements in WUE may occur through reduced gs (e.g. Flaveria [89]). Thus, evolution towards C4 probably first involved a suppression of photorespiration (table 1, phase 2) and then increased PEPC activity (table 1, phase 3), but only this last step enabled a reduction of gs. These steps may even occur within C3 species: populations of the grass Phragmites australis in hot, arid and saline environments show increasing investment in elements required for the C4 cycle, including PEPC, decarboxylase enzymes and bundle sheath tissues, which may enhance both CO2-fixation and WUE [90]. Thus, the engagement of CO2-fixation via PEPC (table 1, phase 3) improves leaf–water relations, allowing a lower value of gs for a given rate of photosynthesis, and thus a smaller absolute response of gs to CO2 depletion in C4 leaves (figure 5b). This benefit would lead atmospheric CO2 depletion and open environments to select for the C4 cycle via plant–water relations, as well as via their effects on photosynthetic efficiency. Together, these physiological differences mean that leaves operating a fully integrated C4 cycle are less prone than C3 leaves to hydraulic failure or stomatal closure in hot, open environments. This contrast in sensitivity to water deficit increases dramatically under atmospheric CO2 depletion.

A greater hydraulic conductance relative to demand, as would arise from the adaptation described, would result in a greater ability to maintain open stomata during soil drying events in C4 than C3 leaves, and a lower sensitivity of stomata to increases in VPD and to decreases in CO2 (see §6). These improvements in water relations provide a plausible physiological basis for the greater likelihood for C4 than C3 grass lineages to invade xeric environments [42].

6. Hydraulic feedbacks on leaf physiology

Our hypothesis that C4 evolved not only to improve photosynthetic efficiency per se, but also to reduce water stress by enabling low gs, has additional implications that at first sight lead to inconsistency. While the C4 species can achieve higher A for a given gs, A declines more rapidly as gs decreases (figure 4a,b). Because of this greater sensitivity of A to gs, a C4 plant must keep stomata open to maintain its advantage in A over C3 plants. At first sight, this problem should render photosynthesis in C4 plants particularly sensitive to soil drying owing to stomatal closure. As an initial test of our hypothesis for a hydraulics-mediated advantage of C4 photosynthesis, and to further explore the physiological implications, we used a novel integrated model of leaf photosynthesis, stomatal and hydraulic systems to compare the physiological behaviour of C3 and C4 species (appendix B), with a particular focus on conditions of CO2 depletion (low CO2), atmospheric water vapour deficit (high VPD) and soil drying (low soil water potential). Given reasonable assumptions, these model simulations supported the hypothesis of a hydraulically based advantage of the C4 syndrome under high VPD and low soil water potential, enabling stomata to remain open, and maintaining A at higher levels than C3 species, with greatest differences at low CO2.

We tested the role of hydraulic conductance in allowing gs and A to be maintained during drought under varying VPD and atmospheric CO2 in C3 and C4 species. We parametrized the model using data from the literature, and coupled this with photosynthesis models for C3 and C4 types (appendix B). Thus, we compared C3 and C4 species that differed in gs (0.23 versus 0.10 mol m −2 s −1 , respectively) but assumed the same responsiveness of gs, and the same vulnerability of the hydraulic system, to declining leaf water potential. We tested three scenarios, with the C4 species having: the same whole-plant hydraulic conductance (Kplant) as the C3 species double the Kplant or half the Kplant (figures 7 and 8).

Figure 7. Simulated response of mid-day operating stomatal conductance (as a percentage of maximum for hydrated leaves) and leaf water potential to drying soil at VPD of (a,b) 1 kPa and (c,d) 3 kPa, for a C3 species and C4 species with identical plant hydraulic conductance (Kplant), for a simulated C4 species with double the Kplant, and for a simulated C4 species with half the Kplant (corresponding to its value of gs being approximately half that of the C3 species). Note that the C4 species maintains stomatal opening into drier soil and higher VPD than the C3. Increasing the Kplant improves this ability in the C4 species, whereas reducing the Kplant by half leads to very rapid decline of gs at high VPD or in a dry soil. (ad) Dashed line, C3 black solid line, C4 light grey solid line, C4, 2 × Kplant dark grey solid line, C4, 0.5 × Kplant.

Figure 8. Simulated response of light-saturated photosynthetic rate to a drying soil at low (20 Pa), ambient (40 Pa) or high CO2 (80 Pa) and VPD of (a) 1 kPa or (b) 3 kPa, for a C3 species and C4 grass species with identical plant hydraulic conductance (Kplant), and for a simulated C4 species with double the Kplant, and a simulated C4 species with half the Kplant (corresponding to its value of gs being approximately half that of the C3 species). (a,b) Dashed line, C3 black solid line, C4 light grey solid line, C4, 2 × Kplant dark grey solid line, C4, 0.5 × Kplant.

When the C4 species had the same Kplant as the C3, the C4 was able to maintain gs at a higher relative level (percentage of its maximum value) as the soil dried this advantage over the C3 was especially strong at higher VPD (figure 7). This result is consistent with an experimental comparison of PACMAD grasses under drought, which showed a more sensitive response of gs to soil water deficits in C3 species than in closely related C4 species [57]. Model simulations also showed lower leaf water potential in the C3 than C4 species as soil dried, until the point of stomatal closure, where the leaves equilibrated with the soil (figure 7). This contrast is also broadly consistent with comparative experiments on closely related C3 and C4 PACMAD grasses, which showed a difference in leaf water potential under moist conditions that was diminished under chronic drought [57,68]. In our model simulations, this advantage was evidently owing to the higher Kplant relative to gs for the C4 over C3 species. When the C4 plant was given double the Kplant of the C3 species, its advantage in maintaining open stomata during soil and atmospheric drought was increased, and when the C4 plant was given half the Kplant of the C3 species, its advantage was diminished.

The ability of a C4 species with similar or higher Kplant to a C3 species to maintain open stomata during drought also translated into an ability to maintain A at a higher level. This advantage went beyond compensating for the tendency of A to decline more precipitously with declining gs in C4 than C3 species, described above (figure 4a,b), and typically provided C4 species with an ability to maintain higher A during mild drought, especially at higher VPD (notably, simulations at yet higher VPDs led to even stronger differences between photosynthetic types). When the C3 and C4 species had the same Kplant, A was higher in the C4 than the C3 under low CO2, but the rank was reversed under high CO2 (figure 8). Doubling the value of Kplant in C4 compared with C3 species gave an advantage in A, and the ability to maintain photosynthesis during drought. This finding is broadly consistent with an early demonstration that, during the dry season in the Negev desert, the C4 species Hammada scoparia showed a shallower decline of A with declining leaf water potential than three C3 species (Prunus armeniaca, Artemisia herba-alba and Zygophyllum dumosum). At a leaf water potential of −6 MPa, H. scoparia (C4) had twice the A of these C3 species [91]. In contrast, when the C4 species in our model simulations had reduced Kplant, this led to a much reduced value of A, and the C3 species showed an advantage of A across all CO2 levels as soil dried minimally (figure 8). These findings indicate that, theoretically, a reduced Kplant in C4 species would annul any advantage of the C4 pathway for photosynthesis under drought or low CO2 in open environments. However, an equal or higher Kplant in these conditions would provide an advantage not only in maintaining open stomata, but also in maintaining a high A, providing a strong benefit to C4 species.

What evidence is there that Kplant is high relative to gs in C4 compared with C3 species? To-date, no studies have made the necessary direct experimental comparisons. Nonetheless, the two comparative studies of five C3 and eight C4 lineages of PACMAD grasses presented in figure 4a (a total of 40 different species) found that C4 grasses generated a lower soil to leaf gradient in water potential (ΔΨ) during typical diurnal transpiration than closely related C3 species [57,58]. Similar patterns have been observed for the C3 and C4 subspecies of Alloteropsis semialata in common garden plots at high irradiance and temperature [92]. This finding is consistent with the hypothesis of a higher ratio of hydraulic supply to demand, i.e. a greater Kplant/gs in C4 than C3 grass species.

Notably, several studies of C4 woody eudicots have suggested the opposite situation, measuring reduced stem hydraulic conductance per supplied leaf area (Kstem) relative to C3 species [93–95]. This was hypothesized to evolve in the final stages of C4 evolution after WUE has increased (table 1, phase 3). A reduced Kstem would not necessitate a reduction of gs under well-watered conditions or mild drought. On the other hand, it would likely reduce xylem construction costs, and also possibly reduce the vulnerability to cavitation of stems, and thus their longevity [93–95]. Such adaptation would be especially important for the economics and protection of long-lived woody parts [93]. However, we note that a lower Kstem does not necessarily imply a lower Kplant indeed, a higher leaf hydraulic conductance (Kleaf) can easily compensate. Recent work has shown the leaf is a critical bottleneck in the whole-plant hydraulic pathway, accounting for greater than 30 per cent of whole plant resistance, and that leaves have steeper hydraulic vulnerability curves than stem [96]. Consequently, Kleaf is a strong determinant of Kplant, especially when leaves begin to dehydrate during transpiration or incipient drought [97–101]. Such an importance of Kleaf in the whole plant pathway is thus consistent with a reduction of Kstem in woody dicot C4 species. It is also consistent with the evolution of high vein density in C3 species under drier climates (table 1, phase 1), which would serve to increase Kleaf and maintain or increase Kplant, while the evolution of higher water storage capacitance would buffer changes in leaf water potential during high VPD or drought [77,96,102,103]. These modifications would then be co-opted for further evolution of C3–C4 intermediates and C4 species (table 1).

In §5, we argued that the low values of gs in C4 species save the hydraulic system from embolism, especially as leaves are heated in open environments, and as stomata are stimulated to open under low CO2. Our model findings further show that the low values of gs in C4 species also reduce stomatal sensitivity to hydraulic feedbacks, allowing stomata to remain open during drought, and photosynthesis to continue, but only if C4 species have similar or higher Kplant than C3 species, and thus a high hydraulic supply relative to demand. A lower Kplant would serve to make C4 species more sensitive to soil drought, especially under high VPD and low CO2. The circumstantial evidence we have presented for grass species is consistent with our hypothesis for a high hydraulic supply relative to demand in C4 species. However, to our knowledge, there are no published data comparing Kleaf for C3 and C4 plants in general, or for grasses specifically. Such data are essential to test our hypothesis.

7. Metabolic limitation of photosynthesis during severe drought

We hypothesized that the evolution of the C4 pathway provides significant physiological benefits for carbon-fixation and water conservation in well-watered soil, during the early stages of soil drought, or during transient drought events. However, there is no a priori reason to expect a greater tolerance of severe desiccation in C4 than C3 species [104]. In fact, recent comparative analyses of closely related C3 and C4 PACMAD grasses suggests the converse that the C4 photosynthetic system may be more prone to greater metabolic inhibition under chronic and severe drought events. Experimental evidence from controlled environment, common garden and field investigations all indicate that photosynthetic capacity declines to a greater extent with leaf water potential in C4 than C3 grass species after weeks of soil drying, or at very high VPD [57,92,105,106]. Chronic or severe drought may thus diminish, eliminate or even reverse the WUE advantage of C4 over C3 species. In the extreme case, photosynthetic capacity is significantly slower to recover after the end of the drought event [106]. Experimental evidence therefore suggests that metabolic limitation of photosynthesis will eventually offset hydraulic benefits of the C4 syndrome during acute or prolonged drought events. For tolerance of severe drought, tight stomatal control and tissue water storage, as is strongly developed in CAM species, or desiccation-tolerant tissue, are far superior to C4 metabolism. However, for tolerance of repeated transient droughts in the growing season, C4 metabolism carries strong advantages, particularly under low CO2.

8. Conclusions

We hypothesized that atmospheric CO2 depletion coupled with high temperatures, open habitat and seasonally dry subtropical environments caused excessive demand for water transport, and selected for C4 photosynthesis to enable lower stomatal conductance as a water-conserving mechanism. C4 photosynthesis allowed high rates of carbon-fixation to be maintained at low stomatal conductance, and reduced stomatal opening in response to low atmospheric CO2. These mechanisms served to reduce strain on the hydraulic system. Maintaining a high hydraulic conductance enabled stomatal conductance and photosynthesis to be sustained for longer during drought events. The evolution of C4 photosynthesis, therefore, rebalanced the fundamental trade-off between plant carbon and water relations, as atmospheric CO2 declined in the geological past, and as ecological transitions drove increasing demand for water.

Our hypothesis adds the evolution of C4 photosynthesis to the list of exceptional innovations based on the plant hydraulic system that arose during periods of low CO2 that have impacted on plant life history, biogeography and the distribution of ecosystems in the deep past, present and future [107]. Previously hypothesized modifications of the water transport system and associated plant features driven by low CO2 include the evolution of xylem vessels and stomata [108], and the planate leaf [109,110] with high vein density [78]. These innovations permitted more rapid growth and diversification, leading to the succession of dominance from pteridophytes to gymnosperms to angiosperms [78,80,111,112]. The evolution of C4 photosynthesis, for improved performance in exposed, seasonally dry habitats in low CO2, thus joins a long line of hydraulic innovations driven by low CO2 that changed plants and the world.


Historical Development and Mechanisms of Evolution and Natural Selection: Early Theories of Evolution

The scientific community has always displayed an interest in the understanding of how life began. A rekindled interest emerged in the 1800s as new geologic and biologic discoveries added to the available knowledge.

Lamarck

Jean Baptiste Lamarck, a French scientist, proposed that species change because of the use or disuse of features, such as tails or arms. He purported the ?use it or lose it? idea. He believed that excessive use of a feature would cause it to grow and lack of use would invite atrophy. He also stated that an individual's increased or decreased features could be passed on to the individual's offspring.

Lamarck hypothesized that acquired traits, not genes, were passed on to offspring. The Lamarckian concept of evolution appeared 50 years before Darwin. Unfortunately, he did not possess an understanding of gene behavior and heredity. However, his ideas started the discussion of evolution in the scientific community and, combined with the three additional ideas that follow, serve as a starting point for Darwin and others.

  • Populations change over time in response to environmental pressure (same as Darwin) and may have evolved from small numbers of starting organisms.
Bionote

According to Lamarck, giraffes grew long necks because they wanted to reach leaves higher up on the tree.

  • Organisms could actively try to change to be more adapted to the environment and then pass that change on to their offspring. For instance, the ancestors of fish saw the advantage of being able to swim faster, so over generations they developed fins instead of legs to increase their speed in water, thereby making them more efficient at getting food and eluding predators. Because this change helped and therefore was desirable to the organism, it was passed on to all offspring.
  • The ?use it or lose it? concept began with Lamarck, who believed that organisms could reshape their bodies in response to a desire to change. Appendages that were no longer needed would not be conveyed to the next generation, whereas other desirable changes could be added.

Many period biologists agreed with Lamarck that these acquired characteristics were inheritable factors. However, with no understanding of genetics, they could not explain how these things could happen.

Lyell

Most people in Darwin's time assumed that the earth was relatively young and that mountains, rivers, and other surface features did not change over time, but were formed by a catastrophic event. For instance, lakes might have formed when a meteorite collided with the earth and then rain filled the resulting crater with water.

Several geologists proposed contrary theories stating that the earth is likely at least four billion years old and that surface features normally change slowly over time. In 1788, James Hutton proposed that the mountains and other surface features gradually change, which supported the hypothesis that the earth was much older than the prevailing thought. Charles Lyell expanded on Hutton's work when he added the concept of uniformitarianism, which stated that the events and processes that created the mountains, lakes, and other surface features are still happening and an understanding of these events was required to explain the formation of existing features. Lyell also proposed that the earth itself had internal movements, as evidenced by earthquakes, that provided further opportunities for change. As scientists began to find and study fossils, Lyell's explanations gained credibility. Lyell contributed to Darwin's thinking in two ways:

  • Past events must be explained in terms of today's events.
  • The earth's history provides ample geologic time for slow change.

Artificial Selection

Darwin realized that a preferred method of selection had been taking place on a local level for a long time. In his conversations with local farmers, he learned that variability exists in every population and was the basis for enhancing yield and productivity. For instance, in a given wheat field, some plants developed greater seeds than others likewise, some cows gave more milk than others. Those individuals that contributed the most, the farmers allowed to reproduce all others were prohibited. In so doing, the farmers were attempting to increase their productivity, and they also selectively favored certain organisms for reproduction. Darwin reasoned that in this form of artificial selection, man could drastically change the appearance of a species in a relatively short period of time from the original wheat or cow to their descendants who were more capable of producing desirable results than their ancestors.

Malthusian Dilemma

Thomas Malthus was actually an English clergyman who worried about the distribution of wealth and resources. His observations and reasoning became known as the Malthusian dilemma, which states that populations multiply geometrically while food sources multiply arithmetically. If left to follow course, the human population would eventually grow larger than the ability of the environment to feed everyone. He predicted large mass starvations that crossed international borders with the possibility of resource wars, famine, and plague. Oddly enough, wars, famine, and plague were the answer to the dilemma, because they served to reduce the reproductive population, an idea that did not escape Darwin. He expanded the phenomenon to all creatures, not just humans, and understood that more offspring are born than will survive to reproduce. Refer to the illustration The Malthusian dilemma.

At point A on the graph, the amount of available resources is adequate to sustain a stable or slightly growing population. At point B, the growth of the human population has reached exponential rates, but the growth of available resources has not increased as dramatically. As a result, Malthus predicted that the intense competition for the resources would lead to war, famine, and plagues.


Watch the video: Plastid Genome Evolution in Solanaceae: past, present and future - Péter Poczai (November 2022).