Is Panmixia very rare?

Is Panmixia very rare?

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I'm reading the wikipidia page on Panmixia.

Panmixia (or panmixis) means random mating. A panmictic population is one where all individuals are potential partners. This assumes that there are no mating restrictions, neither genetic nor behavioural, upon the population and that therefore all recombination is possible. The Wahlund effect assumes that the overall population is panmictic.

In genetics, random mating[4] involves the mating of individuals regardless of any physical, genetic or social preference. In other words, the mating between two organisms is not influenced by any environmental, hereditary or social interaction. Hence, potential mates have an equal chance of being selected. Random mating is a factor assumed in the Hardy-Weinberg principle and is distinct from lack of natural selection: in viability selection for instance, selection occurs before mating.

Now, I would guess from this definition that Panmixia is a condition that almost never occurs, that in the vast majority of cases, there is some sexual selection going on which makes some pairings more likely than others.

But the way the page is written seems to suggest that this is a pretty normal condition of populations, or at lead doesn't mention that it is a "spherical cow" abstraction.

Am I missing something here?

Unravelling population genetic structure with mitochondrial DNA in a notional panmictic coastal crab species: sample size makes the difference

The extent of genetic structure of a species is determined by the amount of current gene flow and the impact of historical and demographic factors. Most marine invertebrates have planktonic larvae and consequently wide potential dispersal, so that genetic uniformity should be common. However, phylogeographic investigations reveal that panmixia is rare in the marine realm. Phylogeographic patterns commonly coincide with geographic transitions acting as barriers to gene flow. In the Mediterranean Sea and adjoining areas, the best known barriers are the Atlantic-Mediterranean transition, the Siculo-Tunisian Strait and the boundary between Aegean and Black seas. Here, we perform the so far broadest phylogeographic analysis of the crab Pachygrapsus marmoratus, common across the north-eastern Atlantic Ocean, Mediterranean and Black seas. Previous studies revealed no or weak genetic structuring at meso-geographic scale based on mtDNA, while genetic heterogeneity at local scale was recorded with microsatellites, even if without clear geographic patterns. Continuing the search for phylogeographic signal, we here enlarge the mtDNA dataset including 51 populations and covering most of the species’ distribution range.


This enlarged dataset provides new evidence of three genetically separable groups, corresponding to the Portuguese Atlantic Ocean, Mediterranean Sea plus Canary Islands, and Black Sea. Surprisingly, hierarchical AMOVA and Principal Coordinates Analysis agree that our Canary Islands population is closer to western Mediterranean populations than to mainland Portugal and Azores populations. Within the Mediterranean Sea, we record genetic homogeneity, suggesting that population connectivity is unaffected by the transition between the western and eastern Mediterranean. The Mediterranean metapopulation seems to have experienced a relatively recent expansion around 100,000 years ago.


Our results suggest that the phylogeographic pattern of P. marmoratus is shaped by the geological history of Mediterranean and adjacent seas, restricted current gene flow among different marginal seas, and incomplete lineage sorting. However, they also caution from exclusively testing well-known biogeographic barriers, thereby neglecting other possible phylogeographic patterns. Mostly, this study provides evidence that a geographically exhaustive dataset is necessary to detect shallow phylogeographic structure within widespread marine species with larval dispersal, questioning all studies where species have been categorized as panmictic based on numerically and geographically limited datasets.


Genetic panmixia, or a complete lack of genetic differentiation across the range of a species, may result when the forces that generate differentiation, such as mutation, selection and drift, are outweighed by the forces that reduce differentiation and increase homogeneity, such as gene flow. Panmixia in natural populations is rare and only expected when gene flow and dispersal are high. For example, Ward et al. [1] examined over 300 animal taxa and demonstrated that differentiation is lowest in taxa with high movement and dispersal capabilities, such as birds and flying insects. Indeed, the major commonality among species in which panmixia has been reported tends to be high movement and dispersal capabilities [2𠄶]. Movement and dispersal capabilities alone, however, are not necessarily good predictors of genetic panmixia [7].

Many avian taxa that have high dispersal capabilities show (sometimes strong) population differentiation, especially when gene flow is restricted by high natal philopatry and behavioural mechanisms [7,8], cryptic barriers to dispersal [9], or local adaptation [10,11]. Reudink et al. [12] and Oomen et al. [13] reported range-wide genetic panmixia in American white pelicans (Pelecanus erythrorhyncos hereafter: pelicans) despite the presence of several predicted behavioural and physical barriers to gene flow. Both microsatellites [12] and mitochondrial markers [13] showed a similar lack of differentiation, suggesting high contemporary and historic patterns of gene flow, respectively. Several other lines of evidence support this idea. First, pelicans can cover hundreds of kilometers while foraging [14] and can disperse long distances. Second, pelicans have recently undergone a large-scale range expansion, including new breeding attempts hundreds of kilometers beyond recent range boundaries into northern Ontario and Nunavut, Canada [15]. Finally, breeding colonies undergo repeated local extinctions and subsequent recolonization events [16], though these events are most often due to abandonment, not mortality. These repeated colony extinctions and recolonization events may re-distribute individuals at broad spatial scales. We suggest that the recent and rapid range expansion of pelicans, e.g., at the eastern edge of their range in Canada, coupled with high levels of gene flow through long-distance dispersal, has likely resulted in an absence of genetic structure. Currently, we lack any information on patterns of breeding dispersal and the provenance of individuals establishing new colonies.

One method for tracking dispersal events is to identify the spatial distribution of genetic variation across the range of the species and assess the origin of colonizing individuals, such as through population genetic assignment tests [17�]. Combined with complementary approaches, such as stable isotope analysis, genetic techniques can sometimes enable delineation of movement patterns (e.g., [21,22]). However, a genetic approach requires at least some genetic structuring among potential source populations to be effective (see [20,23]). Unlike genetic variation, however, variation in biogeochemical markers, such as stable isotopes, is almost entirely dependent on contemporary extrinsic factors (e.g., precipitation, diet) that can vary predictably across the landscape [24,25]. Thus, biogeochemical markers may provide valuable information on movement patterns when genetic approaches are uninformative or indicate panmixia [26]. Here, we examine patterns of range-wide isotopic structuring in the American white pelican to determine whether isotopic signatures of feathers may be informative for creating a species-specific feather isotope basemap, which could be used to examine patterns of dispersal and movement. Because biogeochemical signatures are incorporated into pelican feathers annually during their post-breeding moult, these signatures are determined by the environment at the moult location, offering potential markers for tracking movement patterns at broad spatial scales.

In this study, our aim was to: (a) examine patterns of within- and among-colony variation in three stable isotopes (δ 2 H, δ 3 C, δ 15 N) and (b) examine whether isotopic variation is sufficiently patterned to be used for geographic assignment of unknown individuals to track movement patterns in dispersing pelicans.


Distribution of Perna perna along the Atlantic and Mediterranean Iberian Peninsula

Perna perna was detected at 14 locations out of the 49 surveyed (Fig. 1). Castelejo, southwest Iberia (Portugal), was the northwesternmost location where the Brown mussel was found. North of Castelejo, individuals of this species were not detected, although the mussel Mytilus galloprovincialis was still abundant, indicating the existence of suitable mussel habitat. Into the Mediterranean, both species were reported as far east as Cape Gata, the easternmost limit of the Brown mussel. After a gap along the southeast coast of Iberia where intertidal mussels were entirely absent, only M. galloprovincialis reappeared.

Perna perna range expansion along the Iberian Peninsula. Presence and absence of P. perna are marked by blue and red dots respectively. White dots represent surveyed sites where no mussel beds were found and yellow dots represent the new range limits of the P. perna distribution. The thick blue line illustrates the previously known P. perna distribution along northern Africa. Surveyed locations are described in Supplementary Table S5, from north to south and west to east. Arrow indicates north. The map was created using the open source software QGIS 2.12.3 (

Genetic diversity and genetic structure of P. perna across oceanographic barriers

Mitochondrial DNA – Cox1

Sequences of P. perna (615 bp Cox1 gene) from 730 specimens revealed 127 haplotypes and 112 polymorphic sites (Table 1). PN and LR showed the highest number of overall haplotypes (17) while LP showed the lowest (2), likely due to the very small sample size. BZ and LR presented the highest number of unique haplotypes (8) and KR, CG and CB did not show any unique haplotypes. Whereas 94 haplotypes were private, 33 were shared among populations. Haplotype and nucleotide diversities varied between 0.481 (PM) and 1.0 (LP) and between 0.0010 (PM) and 0.0049 (LP), respectively.

Pairwise ɸST values were non-significant across all locations (P > 0.05 Supplementary Table S1) and ranged from 0 to 0.432 the highest estimate was found between PM and LP. High pairwise ɸST values were recovered from populations with extremely low sampling sizes (e.g. LP, n = 2 0.039–0.432 and SG, n = 4 0.048–0.349).

Spatial analysis of shared alleles (SAShA) indicated that the observed distribution of geographical distance between pairs of haplotypes (OM) was not statistically different from the expectation (EM) under panmixia (OM = 885.30 km, EM = 892.06 km, P = 0.773).

The Akaike Information Criterion corrected for small sample sizes (AICc) selected TrN + G as the best-fit model to be implemented in Arlequin software (gama shape = 0.932). AMOVA analyses attributed most of the variation to within populations (99.52%, P = 0.126 Table 2).

The median-joining haplotype network reconstruction of P. perna revealed one single clade, and no genetic differentiation between a priori expected distinct groups (Fig. 2). The star-shaped network presented two main central haplotypes widespread at all groups. Generally, both shared and private peripheral haplotypes differed from the centre in one or two mutational steps. Haplotypes were shared irrespective of the geographic distance between groups (i.e. haplotypes shared between WM and AI or between WM and WS).

Genetic structure of P. perna across northeastern Atlantic and Mediterranean shores. (a) Oceanographic regions based on dispersal potential simulation of P. perna. Colours along the shore depict distinct oceanographic regions. EM, Eastern Mediterranean WM, Western Mediterranean AS, Alboran Sea AI, Atlantic Iberia NM, Northwestern Morocco SM, Southern Morocco WS, Western Sahara “No mussels” represents areas where the species is either not present (Atlantic central Iberia and northwards southeastern Iberia and northeastwards) or it was not sampled (southernmost coast of the northern African region). Black solid circles represent sampling locations as in Supplementary Table S6. The map was created using the open source software QGIS 2.12.3 ( (b) Median-joining haplotype network of Cox1 gene (left) and bayesian analysis summary plot (each bar represents one individual) obtained from STRUCTURE i.e. K = 1 (right). Circle size is proportional to haplotype frequency. Colours indicate the group origin of a haplotype. Grey line represents the proportion of mutational steps. Coloured bars depict expected genetic clusters.

Microsatellite markers

Out of 732 individuals, 373 alleles were detected in seven loci. The total number of alleles per locus ranged from 12 to 134. Excluding locus P16, there was no clear evidence for large allele drop-out, stuttering or null alleles at a frequency higher than 0.2. Expected (HE) and observed (HO) heterozygosities varied between 0.536 (CB) and 0.796 (LP) and 0.643 (SG) and 0.773 (AN), respectively, resulting in a minor heterozygosity deficit (FIS ranged from 0 to 0.128). Population genetic diversity standardized to the smallest sample sizes, Â(2) and Â(22), varied between 2.714 (LP) and 3.123 (CB) and between 11.966 (IM) and 14.714 (PM), respectively. A total of 105 unique alleles were described with CB reporting the highest number (10 Table 3).

FST and Jost’s D ranged from 0 to 0.034 and from 0 to 0.041, respectively (Supplementary Table S2), and showed no significant differences in any pairwise comparisons (FST lower and upper 95% confidence interval limits ranged from −0.174 to −0.004 and from 0.005 to 0.209, respectively Jost’s D lower and upper 95% confidence interval limits ranged from −0.179 to −0.007 and from 0.022 to 0.279, respectively Supplementary Table S2).

The neighbour-joining tree based on proportion of shared alleles gave clear evidence of the absence of geographical topology (Supplementary Fig. S1).

The log probability of the data (L(K)) returned from the Bayesian admixture analyses implemented in STRUCTURE suggested K = 1 as the best fitting K (Fig. 2). Although using the ΔK method 34 proposed K = 2 as the best fitting K, the two proposed resolved clusters were consistently present at all populations, thus excluding any geographical or genetic separation.

AMOVA indicated that most of the genetic variation arose within populations (99.96% P = 0.728, Table 2).

Discriminant analyses of principal components (DAPC) suggested K = 9 as the best fitting number of clusters. All clusters were distributed across the entire study area, revealing no spatial differentiation among groups (Supplementary Fig. S2).

Simulations of dispersal potential

The Lagrangian particle simulations (LPS) using HYCOM ocean velocity fields over the 11-year period released

3300 particles per cell (32.43e10 6 particles in total). On average, the particles drifted for 110.4 km ± 123.9 (maximum 1019 km) and most connectivity events were produced in the first days of ocean drifting (mean transport time of 2.1 days ± 1.9).

The linear models using ocean connectivity estimates and shortest marine distances failed to explain the genetic differentiation of P. perna, and none had a better ability to explain the data, in terms of either Adjusted R-squared or Akaike criteria (Supplementary Fig. S3).

The identification of oceanographic regions performed with the leading eigenvector algorithm on the stepping-stone connectivity matrix showed a significant modularity value of 0.76 (P < 0.001). The algorithm was allowed to identify 10 distinct regions (Fig. 2), with their breaks in Cape Roca (Western Iberia, Portugal the species is absent from this region), Strait of Gibraltar (Atlantic-Mediterranean meeting point), Cape Gata (southeastern Iberia, Almeria, Spain (Almeria-Oran Front) the species is absent eastward of this break), Oran (Mediterranean northern Africa, Algeria, Almeria-Oran Front), Strait of Sicily (northeastern Africa, Tunisia), Essaouira (northwestern Africa, Morocco), Cape Boujdour (northwestern Africa, Western Sahara) and Cape Barbas (northwestern Africa, Western Sahara no samples acquired south of this break). These break points (i.e., oceanographic barriers) prevented most particles from connecting coastal cells between oceanographic regions during at least one dispersal event (Table 4). With the exceptions of the barriers separating AI from AS (potential to reduce connectivity: 81%), AS from WM (potential to reduce connectivity: 85%) and NM from AS (potential to reduce connectivity: 83%), all oceanographic barriers had the potential to reduce the connectivity between cells by 93% to 100%, with a general increase in reducing connectivity as the relative distance between regions increased (Table 4).

Environmental niche modelling

Pearson’s correlation test revealed strong correlations between sea surface temperature (SST) and surface air temperature (SAT) and between nitrate and phosphate concentrations. Although the discarding of correlated variables may be an arbitrary procedure 35 , the most ecologically representative variables for intertidal species were prioritized in each correlation (e.g. ref. 36), i.e. SST and nitrate concentration. After Pearson’s correlation test minimum and maximum SST, nitrate concentration, salinity, cloud cover and the significant wave height were selected to perform the analyses.

The ensemble produced with the best models (TSS > 0.7) resulted in an accurate overall description of P. perna native distribution, including its expanding front towards southern Iberia (Fig. 3). Along northern Africa, the niche model predicted a distribution from central Senegal north into the Mediterranean, as far as central-eastern Tunisia (Fig. 3). In addition, the prediction indicated that suitable habitat could potentially be found from southeastern Spain to central Portugal. While the probability of P. perna being present on Mediterranean Spanish shores was high, towards the Atlantic the predicted likelihood decreased. On southwestern Iberian shores, the species is absent from several locations where it could be expected. Surprisingly, short portions of potentially suitable habitat were detected along the warm equatorial African coast (in Ghana and Ivory Coast) and the Arabian Peninsula (Yemen and Oman) under the effect of upwelling cells. RandomForest (RF) performed better than other techniques (AUC = 0.939 ± 0.018 and TSS = 0.775 ± 0.044, Supplementary Table S3). The evaluation of the ensemble produced the following ROC-derived scores: AUC = 0.968, sensitivity = 99.099, and specificity = 88.928 TSS = 0.879, sensitivity = 99.099, specificity = 88.839. By obtaining the highest score (0.26), minimum SST was the predictor that best explained the distribution of P. perna (Fig. 3), when modelled alone in comparison with other predictors.

Predicted native distribution for the brown mussel P. perna derived by averaging an ensemble of presence-absence algorithms. (a) overall distribution, (b) P. perna distribution along the expanding front in the Northern Hemisphere, (c) Mean scores of the relative importance of the environmental variables obtained from the ensemble. Blue and red dots represent presence and absence data, respectively, obtained from field surveys and records in the literature (see Supplementary Table S7). The map was created using the open source software QGIS 2.12.3 (

Case study: South Africa

Minimum SST was significantly lower where P. perna is absent compared to where the species is present (all trials P < 0.001, Fig. 4, Supplementary Table S4). In contrast, minimum SAT did not show any significant difference between the two groups of locations (trial 1 P = 0.796 trial 2 P = 0.511 Trial 3 P = 0.063 Supplementary Table S4). Although only one subset is shown, the results were consistent for all three.

Box-plot of minimum sea surface temperature (SST) and surface air temperature (SAT) of the two South African regions where P. perna is absent (cold water) or present (warm water). Box-plot depicts the mean (horizontal line), the standard error (bottom and top of the box) and the standard deviation (whiskers).

Testing local-scale panmixia provides insights into the cryptic ecology, evolution, and epidemiology of metazoan animal parasites

When every individual has an equal chance of mating with other individuals, the population is classified as panmictic. Amongst metazoan parasites of animals, local-scale panmixia can be disrupted due to not only non-random mating, but also non-random transmission among individual hosts of a single host population or non-random transmission among sympatric host species. Population genetics theory and analyses can be used to test the null hypothesis of panmixia and thus, allow one to draw inferences about parasite population dynamics that are difficult to observe directly. We provide an outline that addresses 3 tiered questions when testing parasite panmixia on local scales: is there greater than 1 parasite population/species, is there genetic subdivision amongst infrapopulations within a host population, and is there asexual reproduction or a non-random mating system? In this review, we highlight the evolutionary significance of non-panmixia on local scales and the genetic patterns that have been used to identify the different factors that may cause or explain deviations from panmixia on a local scale. We also discuss how tests of local-scale panmixia can provide a means to infer parasite population dynamics and epidemiology of medically relevant parasites.

T. cruzi Genotypes and its Ecology: A Phenomenon Not Yet Fully Understood

The heterogeneity of T. cruzi had already been observed by Carlos Chagas, who detected slim and wide blood trypomastigotes and, most likely influenced by his experience with malaria, attributed the different forms to male and female merozoites (Chagas, 1909). Later, several authors described different patterns of cell growth and differentiation in axenic cultures, demonstrating that the heterogeneity observed was not only morphological but could result in distinct success in replicating and differentiating into infective forms.

The first attempt to cluster the observed heterogeneity among T. cruzi subpopulations was proposed by Sonia Andrade in the 1970s and was based on the different infection patterns observed in Swiss mice experimentally infected with different T. cruzi strains. Three Biodemes were proposed: Biodeme I for strains that resulted in high virulence and mortality in 10� dpi Biodeme II in the cases of mild virulence and mortality after only 20� dpi and Biodeme III, which resulted in a slow increase in parasitemia and no mortality in infected mice (Andrade et al., 1970 Andrade and Magalh฾s, 1997). This proposition, however, was time-consuming, dependent on laboratory animal availability, and isolates certainly underwent selection pressure due to the experimental infection. Brener (1977) suggested the classification of two polar types based on morphology and tissue tropism, describing an aggressive pole represented by the Y strain and a benign pole exemplified by the CL strain. The biological, immunological, drug resistance and clinical differences that were being unveiled were so impressive that it was even proposed to consider that T. cruzi was in fact a species complex and not a single species and that the taxon should be referred to as the “cruzi complex” (Coura et al., 1966).

The characterization of T. cruzi subpopulations by a biochemical tool was successfully proposed by Michael Miles and coauthors in 1977 based on enzyme electrophoresis (Miles et al., 1977). This proposition was certainly one of the most important landmarks in the study of T. cruzi biology, and the three main zymodeme groups proposed (Z1, Z2, and Z3) were the basis for the first nomenclature consensus proposed in 1999 (Anonymous, 1999). Another important zymodeme described in the Southern Cone of South America was the so-called Z2 Bolivian or Zymodeme 39 (named TcV in the current T. cruzi nomenclature), which is a hybrid parasite that is the result of a natural product of meiosis recombination between the parentals TcII and TcIII. This T. cruzi genotype was described by its heterozygous profile of the isoenzyme glucose phosphate isomerase, which gave important information long ago (Apt et al., 1987 Brenière et al., 1989). The majority of the molecular studies on T. cruzi that started to be conducted approximately a decade later confirmed the differentiation into the two main (and parental) groups, T. cruzi TcI (Z1) and TcII (Z2) (Clark and Pung, 1994 Tibayrenc, 1995 Souto et al., 1996).

Since their description, the different zymodemes were associated with different transmission cycles: Z1 and Z3 were associated with the transmission cycles in the wild and Z2 in the domestic environment. The domestic cycle of T. cruzi transmission was proposed to be somewhat independent from the sylvatic one, although sometimes overlapping (Miles et al., 1980 Apt et al., 1987 Zingales et al., 1998). This proposition was supported, in part, by two important features: (i) T. cruzi TcI (Z1) is the most ubiquitous subpopulation and, because of that, is the most frequently detected subpopulation in the wild (Fernandes et al., 1999 Noireau et al., 2009 Jansen et al., 2015) and (ii) T. cruzi TcII (Z2) was the subpopulation that was consistently isolated from human cases in the formerly endemic areas of Central Brazil, especially maintained by T. infestans in indoor transmission. This subpopulation was therefore associated with the domestic cycle of T. cruzi transmission and with the severe clinical conditions that occurred in 30% of the infected people (Chapman et al., 1984 Fernandes et al., 1999). It was more than two decades later, through the description of a well-established transmission cycle involving free-ranging golden lion tamarins (GLTs Leontopithecus rosalia) and T. cruzi Z2 subpopulations (later confirmed as DTU TcII), that this association was challenged (Lisboa et al., 2000, 2006). Moreover, the infection by T. cruzi TcII in GLTs was followed up for more than a decade and was demonstrated to be the most stable and expressive transmission cycle of this DTU in the wild (Lisboa et al., 2015). Since these initial findings, T. cruzi DTU TcII has been described in several other wild mammal species throughout Latin America, including rodents, marsupials, bats and carnivores (Jansen et al., 2015). To date, it has not been possible to unequivocally associate T. cruzi genotypes with any biological response variable, including the biome and environment (as first proposed) or host species (as proposed secondly).

The advances of the molecular techniques for T. cruzi characterization since the late 1980s, and the most diverse targets proposed, showed that T. cruzi heterogeneity was much higher than the biochemical studies could reveal and made it possible to study the parasite at a much higher level of detail. Soon after the first nomenclature consensus was published, six discrete phylogenetic lineages (later named discrete typing units𠅍TUs) were proposed (Brisse et al., 2000). The former Z1 and Z2 comprised one DTU each, Z3 was divided into 2 distinct DTUs, and the hybrid isolates were grouped into two other DTUs. This division was based on the second (and currently valid) nomenclature consensus that divided the T. cruzi subpopulations into 6 DTUs, named TcI to TcVI (Zingales et al., 2009). A putative seventh DTU, Tcbat, was described as a DTU associated with bats, although human infections by this DTU were already reported (Marcili et al., 2009 Guhl et al., 2014 Ramírez et al., 2014).

It is not surprising that TcI was initially associated with the sylvatic cycles because TcI is the most widespread DTU, being detected in all areas of T. cruzi transmission (Jansen et al., 2015). This DTU was first associated with opossums however, while individuals from the Didelphis genus were most commonly infected by TcI (Fernandes et al., 1999 Jansen et al., 2015 Roman et al., 2018b), individuals from the Philander genus were found to be infected by both TcI and TcII at similar rates (Fernandes et al., 1999 Pinho et al., 2000 Jansen et al., 2015). T. cruzi TcII infection may be detected in concomitant infection with TcI in Didelphis individuals (Jansen et al., 2018). The proposed association among TcI, Didelphis sp. and the arboreal stratum (Yeo et al., 2005) did not consider that Didelphis spp. are scansorial and not arboreal mammals, i.e., Didelphis sp. may also use the terrestrial and arboreal strata. This DTU, along with DTUs III and IV, is involved in human cases in the Amazonian basin, currently the region that reported more than 90% of new cases in Brazil and severe acute phases (Monteiro W. M. et al., 2010 Monteiro et al., 2012).

The DTU TcII included T. cruzi subpopulations derived from patients from formerly endemic areas, where clinical symptoms of chronic Chagas disease were common and severe, and because of that, this DTU was associated with a domestic cycle of parasite transmission. Reports on TcII-infected wild mammals are less numerous in comparison to those on TcI, but TcII also presents a noteworthy host range and is widely distributed in nature (Jansen et al., 2015). TcII is the second most frequently found genotype infecting wild mammals in Brazil, including mammals of the Amazon basin region (Lima et al., 2014).

Undoubtedly a turning point, an important milestone in the discussion of genetic diversity in T. cruzi was the recent description of panmixia in some T. cruzi subpopulations (Schwabl et al., 2019). The description of this phenomenon in some isolates of Ecuador sheds light on a decades-long debate related to the largely clonal character of the taxon. More intriguing is the description of clonal groups that may occur in sympatry with clonal groups that the authors propose to have experienced in past hybridization events. These fascinating findings largely explain the extreme diversity of T. cruzi and its extreme adaptability to species and tissues of its numerous vertebrate and invertebrate hosts Additionally, the studies of Schwabl and coauthors postpone further the possibility of understanding the ecological significance of the genetic diversity of T. cruzi (Schwabl et al., 2019).

Is Panmixia very rare? - Biology

Discovering the genes that underlie phenotypic variation within species is increasingly common, but figuring out how they respond to natural selection is a major challenge. Stickleback researchers have been particularly successful at identifying genes or genomic regions of major phenotypic effect. The Pitx1 gene, for example, is known to influence pelvic girdle and spine development. QTL studies have revealed genomic regions underlying variation in phenotypes ranging from juvenile growth rate, gill rakers, pigmentation, schooling, and sensory systems. The Ectodysplasin gene (Eda) is particularly interesting, because of its strong effect on the number of bony lateral plates in stickleback (Colosimo et al. 2004). Multiple freshwater stickleback populations have a reduced number and/or size of lateral plates relative to their marine ancestors, suggesting that natural selection has repeatedly acted on Eda following the colonization of freshwaters by stickleback.

Over a decade has passed since the discovery of Eda, and numerous speculative hypotheses have emerged about what selective forces affect Eda to control armor plate evolution in wild stickleback populations. In 2008, Barrett and colleagues did a selection experiment with the aim of observing how colonization of freshwater could drive phenotypic evolution of stickleback armor (Barrett et al. 2008). They introduced marine stickleback, heterozygous at the Eda locus, into freshwater ponds and found strong positive selection for the low-plated Eda allele. As predicted, the low-plated phenotypes had a fitness advantage once lateral plates had developed, possibly due to enhanced growth in freshwater environments (Marchinko and Schluter 2007). However, in early life stages (prior to plate development) selection favored the high-armor (“complete”) allele, suggesting that the strength and direction of selection varied among life stages. They concluded that Eda was potentially having either direct or epistatic effects on other phenotypic traits affecting fitness. As simple as this experiment was, it revealed considerable complexities about how natural selection drives phenotypic evolution, even when the phenotype has a relatively simple genetic basis.

Prior to this experiment, Marchinko and colleagues had begun to investigate a polymorphism in body armor of a population of stickleback in Kennedy Lake on Vancouver Island. Plate polymorphisms are not unique to Kennedy Lake, but in the Pacific basin it is relatively uncommon to have a high frequency of both completely plated and low-plated individuals. Typically, freshwater populations are either low-plated or fully plated. In some cases, a polymorphism is present transiently, as the frequency of plates changes over time in response to changing selection pressures (Kitano et al. 2008). In Kennedy Lake, however, this plate polymorphism has been stable since at least 1965.

Typically, polymorphisms are thought to be maintained either by heterozygote advantage (when the fitness of Aa is higher than that of both AA and aa genotypes), or more commonly by spatially varying selection (whereby each of AA and aa have highest fitness in different parts of the population). In contrast, population genetic theory indicates that a polymorphism is highly unlikely to persist when heterozygotes have a disadvantage (when the fitness of Aa is lower than AA or aa). This is because in the absence of assortative mating, a higher fraction of copies of whichever allele is rarest (A or a) end up in low-fitness heterozygotes. Selection is expected to drive the common allele to a frequency of , eliminating the polymorphism. With the discovery of Eda’s effects on lateral plates, the Kennedy population became an attractive system to test the role of natural selection in maintaining a polymorphism.

The first hint that something interesting was going on in the Kennedy Lake stickleback population came from our first sampling campaign in 2004. We found that the vast majority of individuals were low-plated or completely plated, whereas intermediates were scarce. Low-plated and completely plated morphs differed both in their morphology (head shape) and stable isotopes (reflecting diet/habitat choice). The results were difficult to interpret, as we had no strong a priori prediction about how diet or morphology might differ between the morphs.

The story became much more interesting when we started genotyping. Over multiple years of sampling the adults in the population, we repeatedly found a deficit of Eda heterozygotes that was not associated with population structure. This indicated that the polymorphism was unlikely to result from either heterozygote advantage or gene flow between locally adapted populations. Maybe assortative mating could explain the heterozygote deficit? Not so. We raided egg clutches from stickleback nests and found they were in Hardy-Weinberg equilibrium.

Without evidence for assortative mating, the most likely explanation was that every year disruptive natural selection regenerated the heterozygote deficiency in the adult population. We estimated that heterozygotes were 20󈞊% less fit than individuals with the fully plated homozygous genotype, and up to 80% less fit than the low-plated homozygous genotype. The low fitness of the heterozygotes has been observed only once before, in a previously published experiment by Zeller et al. (2012). The superior fitness of the low-plated homozygous genotype was consistent with an observed growth advantage of this genotype in a previous study (Marchinko and Schluter 2007).

At this point we had some nice patterns from a single stickleback population, but why is this interesting to non-stickleback folk? First, evidence for stable genetic polymorphisms with heterozygote disadvantage are extremely rare, even though theory suggests that they might arise under a wide range of ecological conditions. Second, the polymorphism appears to be maintained under a seemingly worst-case scenario. As we described above, maintenance of a polymorphism with heterozygote disadvantage is theoretically difficult. However, the solution might be frequency-dependent selection: each allele might have an advantage overall as it becomes rare. Third, such a polymorphism can lead to a wide range of evolutionary outcomes, including the evolution of dominance, assortative mating (and possibly sympatric speciation), or the loss of the polymorphism. Although the specific outcome is difficult to predict, Kennedy Lake sticklebacks are well suited for studying how frequency-dependent selection can maintain genetic and phenotypic diversity within a population.

Our study also adds another chapter to the Eda story. The mere existence of the stable polymorphism means that fully plated and low-plated populations are not the only options. However, we still know very little about the agents of selection that affect Eda in natural populations, and so we can only speculate about the forces driving disruptive selection (and rare-allele advantage, if it exists) in the Kennedy Lake population. Hopefully our study has exposed our ignorance and will inspire further experimental tests and new comparative studies of polymorphic stickleback populations.

Global phylogeography of sailfish: deep evolutionary lineages with implications for fisheries management

Since the Miocene profound climatic changes have influenced the biology and ecology of species worldwide, such as their connectivity, genetic population structure, and biogeography. The goal herein is to evaluate the phylogeography of sailfish Istiophorus platypterus between the Atlantic, Indian, and Pacific oceans. Our results evidenced a high genetic diversity and three distinct populations among the ocean basins with limited gene flow among them. In addition, the species is characterized by two deep evolutionary lineages that diverged during the Miocene/Pliocene transition, one of them is circumtropical while the other is restricted to the Atlantic Ocean. These lineages evolved along the successive glacial-interglacial cycles from the Pleistocene and remained isolated from each other in glacial refugium until deglaciation. Assessments of sailfish suggest it may be subject to overfishing and the results herein imply the need to re-evaluate the current stock delimitations and management measures adopted by the Regional Fisheries Management Organizations, especially in the Atlantic and the Indo-Western Pacific oceans to effectively manage the species. In addition, this work highlights that both lineages should at least be treated as two distinct management units in the Atlantic Ocean until their taxonomic status is fully resolved, given their high genetic divergence.

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The authors wish to thank all who assisted in sampling of seabirds: Tracy Anderson (Save Our Shearwaters), Nicole Galase (Pōhakuloa Training Area Natural Resources Office), Molly Hageman (Bernice Pauahi Bishop Museum), Dr. David Hyrenbach (Hawai‘i Pacific University), and Dr. Andre Raine (Kauai Endangered Seabird Recovery Project). We further thank colleagues at the Toonen-Bowen Laboratory and Hawai‘i Wildlife Ecology Laboratory for assistance throughout the project.


Phylogenetic relationships among early embryophyte lineages

It has been recognized for over a century (e.g., 97 ) that the green algae (Chlorophyta plus streptophyte algae) share significant structural and biochemical features with land plants (bryophytes and tracheophytes embryophytes). The green algae, however, are heterogeneous and include taxa in which one or the other or both generations are multicellular, so inferences about the origin of the embryophyte life cycle depend on which group of green algae is sister to the embryophytes ( 46 86 ). Evidence from ultrastructural, biochemical, and molecular data supports the view that the charophycean green algae (including the Charales, Coleochaetales, and other groups) are closely related to the embryophytes, and so their life cycles are informative about the ancestral condition in embryophytes. The charophycean algae themselves include early-diverging unicellular types such as Mesostigma viride Lauterborn. Phylogenetic evidence supports close relationships between embryophytes and several charophycean groups, the Zygnematales ( 155 ), Coleochaetales ( 43 ), and Charales ( 62 98 99 ). The modern green algal group most closely related to embryophytes is unclear at the present time ( 2 ). While it is clear that in general multicellularity has evolved multiple times (i.e., among protistan groups), all candidate sister groups to the embryophytes are characterized by a haplobiontic life cycle in which the gametophyte is multicellular and dominant and the sporophyte generation is limited to a unicellular zygote. Thus, the multicellular sporophyte characteristic of all embryophytes appears to have evolved by interpolation of mitotic cell divisions prior to meiosis. This scenario in which the sporophytes of land plants represent an evolutionary innovation corresponds to the so-called antithetic theory concerning the evolution of the embryophyte alternation of generations ( 9 ). Nevertheless, significant questions remain about the nature of the sporophyte in the early ancestors of extant embryophytes (see below).

Multiple lines of evidence suggest that the three bryophyte clades (liverworts: Marchantiophyta mosses: Bryophyta and hornworts: Anthocerophyta) form a paraphyletic grade basal to the tracheophytes, although some data, including both morphological ( 36 ) and molecular ( 87 ), suggest that either the mosses and liverworts form a monophyletic group, or all three groups form a single clade. 99 and 98 have shown that the distribution of mitochondrial group II introns across groups, in addition to considerable sequence data, strongly supports the paraphyly hypothesis, and that the branching order at the base of the embryophyte clade is liverworts, then mosses, then hornworts, and then the tracheophyte crown group. This view serves as a well-supported working hypothesis for early land plant relationships (Fig. 1).

Working hypotheses for relationships among major clades of land plants. Alternative scenarios for the evolution of land plant sporophytes are shown on the figure. “A” at each node represents a relatively undifferentiated but multicellular sporophyte “B” shows an unbranched, monosporangiate sporophyte “C” shows a dichotomously branched sporophyte. The key (upper left) suggests three general scenarios that could have occurred for example, ancestral states for the three nodes (a, b, c) could be A-A-A, which implies independent evolution of complex sporophytes from ancestors with little differentiated but multicellular sporophytes. Other possible scenarios, including various reversals, are of course also possible.

Spore and tubular remains with apparent liverwort affinities from the Ordovician Period some 470 million years ago (Ma) suggest that at least some of the earliest land plants may have had a heteromorphic haploid-dominant alternation of generations like modern liverworts (reviewed by 37 86 ). Spore diads that appear to be intermediate between those of extant Coleochaete species and embryophytes are known from the Cambrian Period ( 154 ). Later, morphologically similar axial gametophytes and sporophytes from Devonian strata of the Rhynie Chert (ca. 410 Ma) suggest that there was a period in early land plant history when sporophyte and gametophyte generations were isomorphic ( 63 153 ). The fossil evidence is thus consistent with a scenario in which plant life cycles may have followed a trajectory from haploid- to diploid-dominant via an isomorphic transitional stage.

But what was the nature of the sporophyte generation in the common ancestors of liverworts, mosses, and hornworts? We still do not know how complex the sporophyte was in the common ancestor of extant liverworts, mosses, or hornworts, nor of subsequent ancestors prior to the origin of tracheophytes (Fig. 1). Stated differently, questions remain about the homology of sporophytic structures in these groups. It is possible, for example, that the common ancestor of all embryophytes had a very simple, even if multicellular, sporophyte and that the sporophytes of living bryophyte phyla, with more or less differentiated vegetative and sporangial tissues, represent independent evolutionary innovations. Conversely, there is paleobotanical evidence that the common ancestor of tracheophytes was characterized by equally complex gametophyte and sporophyte generations (i.e., an isomorphic alternation of generations), and it could be that complex sporophytes evolved early in embryophyte evolution with parallel reduction in liverworts, mosses, and hornworts (Fig. 1). The history of plant life cycle evolution probably lies somewhere between these extremes wherein sporophytes of the bryophyte phyla represent independent innovations from ancestors of intermediate complexity, and the degree of homology depends on the extent to which sporophyte elaboration used a common genomic “toolkit”, vs. truly independent evolution from scratch. The sporophytes of mosses, liverworts, and hornworts are very different, despite the fact that in all three groups they are unbranched and monosporangiate. Those of liverworts, for example, lack stomata and have no specialized photosynthetic tissues (although epidermal cells contain chloroplasts at early stages of development). The setae of liverworts are very simple in structure and highly ephemeral (usually lasting only days). The sporophytes of mosses typically persist for longer periods, have greater anatomical complexity, and the sporangium usually has specialized photosynthetic tissues and stomata. The linear sporophytes of hornworts lack differentiated setae but have photosynthetic tissues and stomata. Sporangial dehiscence also differs among the three groups, and the sporophytes develop in radically different ways by diffuse cell divisions in liverworts, apical and intercalary growth in mosses, and a basal intercalary meristem in hornworts. Water-conducting cells occur in the sporophyte of mosses but not liverworts ( 70 ). Thus, despite (presumably plesiotypic) similarities, it is conceivable that the multicellular sporophytes of liverworts, mosses, and hornworts evolved largely in parallel from ancestors with less complex sporophytes.

Gene expression and the evolution of plant life cycles

The most intriguing aspect of the alternating sporophyte and gametophyte generations of land plants is their extreme morphological and functional divergence despite having shared genomes. Although the two generations differ in their ploidal level, this difference alone does not lead to the development of different structures. That other factors are involved is well shown by early evidence of apogamy and apospory ( 29 97 ) in which abrupt switches between generation-typical morphologies and function are not associated with ploidal changes brought about by syngamy or meiosis. Phenotypic and functional divergences between the two generations clearly arise by differential usage of the same genetic material.

Accumulating evidence suggests that morphological and functional transitions between sporophyte and gametophyte are achieved by drastic reprogramming of gene expression patterns through generation-specific transcription factors (reviewed by 127 69 24 ). The evolutionary origin of diplobiontic life cycles from a purely haplobiontic life cycle required the evolution of regulatory mechanisms governing developmental and physiological processes of the new generation, the multicellular sporophyte. Similarly, the transition from a haploid- to diploid-dominant alternation of generations must have been accompanied by radical changes in regulatory mechanisms enabling large-scale changes in function and morphology of both generations. Genomic mechanisms underlying sporophyte development could have evolved de novo or by the partial or full transfer of preformed gametophytic programs to the sporophyte generation ( 88 24 86 ).

Studies investigating the effect of major regulatory gene homologs of Arabidopsis thaliana in the model moss Physcomitrella patens are consistent with the transfer of gametophytic developmental programs to the sporophyte generation. An impressive example is provided by ROOT HAIR DEFECTIVE 6 (RHD6)-like transcription factors regulating root hair development in Arabidopsis thaliana and rhizoid development in the moss Physcomitrella patens ( 76 ). Here a complete regulatory toolkit appears to have been recruited from the gametophyte for similar functions in sporophytes. Genes and genetic networks involved in the development of reproductive structures across land plants appear to have followed a similar evolutionary path. MADS box genes are preferentially expressed in gametangia and in the basal part of the moss sporophyte. Furthermore, their defect leads to abnormalities related to the development of reproductive structures in mosses ( 100 169 reviewed in 128 ). In Arabidopsis, MADS box genes have similar functions and expression patterns as key regulators of the reproductive phase, with expression restricted to the formation of reproductive structures ( 12 ). Similar expression patterns and functions suggest that MADS box genes are conserved across land plants and that gametophyte developmental programs were recruited to the sporophyte to perform similar functions.

Regulatory genes and networks underlying critical adaptations to the terrestrial environment may have first appeared in the dominant gametophyte generation and later transferred as the sporophyte was elaborated. Comparative analyses of desiccation and salt tolerance across land plants have revealed conserved regulatory networks acting in the moss gametophyte and angiosperm sporophyte, providing further evidence for the genomic transfer of gametophytic programs to the sporophyte ( 64 108 ).

Comparative analyses of regulatory genes expressed mainly in the sporophyte generation of Arabidopsis thaliana and Physcomitrella patens shed light on regulatory mechanisms that likely evolved de novo during the course of land plant evolution. Class I KNOX genes are expressed only in the sporophyte generation of mosses, ferns, and angiosperms, and in the latter two groups, they are important in the development and maintenance of the shoot apical meristem ( 51 ). In Physcomitrella patens, they are expressed in the developing sporophyte, and their defect leads to the abortion of the sporophyte, but they cause no detectable abnormalities in gametophytes ( 112 127 ). Another example is provided by LEAFY/FLORICAULA genes that have an important role in the formation of the floral meristem in angiosperms ( 84 ). LEAFY homologs in the moss Physcomitrella patens are key regulators of the sporophytic stage by regulating the first division of the zygote. Although these genes are expressed in both generations, they have no detectable effect on the development of gametophytes in Physcomitrella patens ( 150 ). Auxin-regulated axis development also appears to have evolved de novo in connection with the origin of the sporophyte generation. Polar auxin transport is only present in the sporophytes of bryophytes and angiosperms ( 95 35 34 ). Finally, genes in the Prc2 complex (FIE, CLF) of Arabidopsis thaliana and their moss homologs prevent parthenogenetic formation of sporophytic tissues, and this role appears to be conserved across land plants ( 80 89 ). Although studies on the evolution of developmental programs across basal and derived groups of land plants has significantly increased during the last 10 years, available information is still fragmentary and is focused on relatively few developmental genes with major effects in angiosperms. The proportions of regulatory genes and gene networks acquired by sporophytes via functional transfer from gametophytes, vs. de novo evolution in the embryophyte sporophyte, are poorly known.

Monitoring transcriptional changes associated with the gametophyte–sporophyte transition could help to understand how generation-specific morphologies and functions are achieved by the reorganization of gene regulatory networks. Moreover, comparative analysis of generation-biased gene expression across land plants can provide critical insights into the origin of embryophytes and the evolution of plant life cycles on a genome-wide scale. Toward this end, we are currently investigating genome-wide, generation-biased gene expression patterns in Funaria hygrometrica (a close relative of the model, Physcomitrella patens) using next-generation sequencing of mRNA and conducting comparative analysis of generation-biased gene expression across land plants ( 145 ). In a comparison of expression profiles from the gametophytes and attached isogenic sporophytes derived from intragametophytic selfing, genes in Funaria fell into three natural groups. (1) Genes with “generation-specific” expression (2) those with “generation-biased” expression and (3) those with “similar expression” in both generations. From the 558 differentially expressed genes, similar numbers were differentially expressed toward the two generations there were 277 gametophyte- and 281 sporophyte-characteristic transcripts (both generation-specific [group 1] and generation-biased [group 2] genes). Overall, ca. 70% and 68% of the generation-characteristic genes fell into the biased category.

Comparative analyses of generation-biased gene expression in A. thaliana and F. hygrometrica shed light on crucial questions related to the origin and evolution of land plants and are briefly summarized here ( 145 ). Our findings show that a large proportion of genes is expressed in both the gametophyte and sporophyte generation in Funaria. In particular, we found that the proportion of transcripts with generation-biased gene expression (2.5% gametophyte, 2.5%, sporophyte) is lower than in Arabidopsis. Furthermore, the similar proportion of sporophyte- and gametophyte-biased genes suggests less gene expression specialization between generations in the bryophyte system compared to angiosperms, where the distribution of generation-specific gene products is unequal (∼5% and ∼25% in gametophytes and sporophytes, respectively). The extensive overlap and weak specialization in gene expression between the two generations is in agreement with the origin of alternation of generations from an algal ancestor with a purely haplobiontic life cycle. Our data suggest that extensive sharing in gene expression between generations may have been the rule rather than the exception in earliest land plants.

We compared expression patterns between Funaria gametophytes and Arabidopsis sporophytes, as well as between sporophytes in the two model systems. Our analyses show that there is limited conservation of generation-biased gene expression between the moss and angiosperm, suggesting extensive intergenerational transfer of genetic networks. Furthermore, extensive overlap in gene expression between bryophyte gametophyte and angiosperm sporophyte generations implies that their morphological and functional similarity is not superficial. It relies on the shared usage of a common set of orthologous genes, indicating that multiple gene networks of the sporophyte generation may have been acquired from the gametophyte by intergenerational transfer.

We found poor gene expression conservation between the sporophyte generations of Arabidopsis and Funaria, suggesting that angiosperm and bryophyte sporophytes diverged in an early stage of sporophyte evolution, with subsequent parallel evolution of many important gene networks characterizing the sporophytes of extant groups. Nevertheless, the core set of sporophyte-expressed transcripts mainly consists of genes critical for terrestrial life (enhanced osmotic regulation, stress, desiccation and UV tolerance, transporters, and intercellular communication via hormones). Therefore, biological processes underlying molecular adaptation to terrestrial life may have already been used by early sporophytes. These adaptations may have contributed to the successful evolutionary diversification of the sporophytic generation in the terrestrial environment.

Our data do show that a significant proportion of preferentially sporophyte-expressed transcription factors in the model moss have orthologs in A. thaliana known to function in the shoot apical meristem and in development of reproductive structures. This similarity in control mechanisms suggests that in spite of considerable morphological and developmental divergence, similar basic regulatory networks are likely to be involved in growth and reproductive tissue development in the moss and angiosperm sporophyte generation. Moreover, the presence of orthologous transcription factors with putatively shared functions in the developmental processes of both reproductive and vegetative sporophytic tissues/organs implies that both domains may have already been present in the common ancestor's sporophyte. Overall, our data suggests that the common ancestor may have possessed a morphologically simple sporophyte nevertheless adapted to terrestrial life and possibly with differentiated vegetative and reproductive tissues (possibly corresponding roughly to the A-A-A sequence of ancestral sporophytes in Fig. 1).

This work was supported by the Fundamental Research Funds for the Central Universities (No. 2019ZY32), the National Nature Science Foundation of China (No. 31972948) and the Program of Introducing Talents of Discipline to Universities (111 Project, No. B13007). The funding body had no role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.


Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China

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