Two-fold cost of sex and r/K selection theory

Two-fold cost of sex and r/K selection theory

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This article cites a bunch of articles (I haven't been through them) that the effect of the two-fold cost of sex is "reduced" in stable environment or in K-selected environment. It says:

[… ] the infamous 'two-fold' cost may be reduced or, perhaps more accurately, more easily balanced in K-selected species. The 'cost of males' is with respect to reproduction. Abugov (1985) argued from life history theory principles that the two-fold cost of sex might be easier to pay with K-selection. The two-fold fecundity advantage of asexual reproduction is always a two-fold fitness advantage, regardless of whether it is in a K- or r-selected environment. However, a survival advantage is worth more under K-selection than under r-selection. Consequently, it is easier to balance the two-fold cost under K-selection if sexually derived genotypes have a survival advantage.

I think that k-selection, k-selected environment and stable environment describe (more or less) the same kind of environment. Let me know if this sounds wrong to you. Here is wiki for r/K selection theory

From the same article K-selection is defined as:

K-selection might favour slower development, greater competitive ability, delayed reproduction, higher survival rates, lower resource thresholds, leading to 'efficiency' (rather than productivity) and constant population sizes at or near carrying capacity of the environment.

It sounds really strange to me. Can you please help me to understand why the two-fold cost of sex is lower in stable environment than in unstable environment?.

r/K selection has become more of an heuristic for characterizing a species' strategy of reproduction and less a matter of predicting what sort of species will emerge from a given environment as it had originally been proposed by MacArthur and Wilson in 1967. The paper you cite tries to determine whether rotifers become more r or more K selective in different environments.

The thought here on k-selection is not almost from the definitions of the term, which is why it isn't explained in the paper.

In R-selected strategies, many more offspring are produced, but less investment is made in each one. Think about a cockaroach laying thousands of tiny eggs. The hatchlings might be eaten by their own mother; they are so 'cheap' the insect who layed the eggs doesn't have any anxiety about their survival. In extreme cases, most of these hatchlings will not reproduce, they may even be a bit of food for the ones which do reach maturity.

In k-selected strategies, very few offspring are produced. In addition to the 'cost of sex' limitation, they are invested in so heavily that the female may stop being fertile for a while. An example would be how female mammals which are lactating are not fertile or seasonal mating like many birds do; the females turn off reproduction so that they can focus on the success of one or two produced offspring.

k-selection is advantageous over R-selection when more of their investment pays off. If one out of ten R-offspring survive and one out of four k-selected offspring survive, then for these competing rotifers, the k-selected strategy is advantageous.

The cost of sex is that its half as efficient as asexual reproduction because males don't really reproduce - they only provide genetic material for females. You can argue r/K selection independently of this factor, but the article is suggesting that k-selection can be so advantageous as to also give sexual selection an advantage over asexual selection. I think asexual reproduction could be k-selected as well, but that seems to be the point being made here.

The reason that k/R has toned down in importance in the past couple of decades is that it has been found that individual species can adapt to shift their k/R strategems.

Testing the hypothesis of sexual selection using genome editing

We identified a gene underlying male-specific red coloration of pectoral fins in the Oryzias woworae medaka fish. Using genome-edited fish, we tested whether the red males attract more females and predators than non-red males.


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Antler's horns, stag beetle's mandibles, and stickleback's red throats: how such conspicuous male display traits have evolved? Since Charles Darwin proposed the theory of sexual selection about 150 years ago (1), many behavioral studies have been conducted to test the theory of sexual selection. In contrast, little is known about the genetic basis for the evolution of male ornaments and armaments. What are the causative genes and mutations underlying the evolution of male conspicuous display traits? In Ansai et al. 2021 in Nature Communications (2), we tackled this question using a beautiful tropical medaka fish (rice fish) (Fig. 1).

Fig. 1. Oryzias woworae (upper, male lower, female). Photo by N. Hashimoto (Aqualife).

When I was a postdoc, I found that variation in sexually dimorphic dorsal spine length and dorsal pricking courtship behavior were linked to a neo-sex chromosome in sticklebacks (3). This led me to hypothesize that neo-sex chromosome evolution may be linked to the evolution of sexual dimorphism. When I had my own lab in the National Institute of Genetics, Japan in 2011, I decided to test this hypothesis using other species.

While I spent my days working on sticklebacks in Seattle as a postdoc, Dr. Kazunori Yamahira was working on the latitudinal cline of life history traits of Japanese medaka fishes as an Associate Professor of Niigata University, Japan (4). We met for the first time at Evolution 2005 in Fairbanks, Alaska. At that conference, I was very impressed by Kazunori's beautiful work. Five years later, I returned to Japan and started to get in touch with Kazunori (currently in Tropical Biosphere Research Center of University of the Ryukyus). With a long-term interest in the mysteries of amazing biodiversity in tropics, Kazunori had started to work on the tropical medaka fishes. Although he was interested in the genetic basis for the biodiversity in tropics, he had no expertise in genetic and genomic technologies at that time. Through discussion, we realized that our expertise was complementary and that Indonesian medaka fishes can be a great model for investigating the link between sex chromosome evolution and sexual dimorphism. When Kazunori showed a beautiful medaka fish, Oryzias woworae (Fig. 1), I immediately liked this beautiful fish. The red coloration of the pectoral fin is unique to the male of this species and no other Oryzias fishes have such red pectoral fins.

While Kazunori and I were discussing such collaborations, Dr. Satoshi Ansai spent his days as a PhD student in Kyoto University applying newly emerged genome editing technologies to the Japanese medaka fish (5). Satoshi optimized the technology in the medaka and collaborated with many developmental biologists and neuroscientists. When Satoshi almost finished his PhD, he thought that it would be exciting to apply the genome editing technologies to the study of ecology and evolution of natural populations. Satoshi contacted me in 2015, was very excited about the project on the Indonesian medakas, and decided to join my lab. Since then, Satoshi, Kazunori and I have been collaborating over 5 years.

Fig. 2. Fotuno oe (a habitat of Oryzias woworae).

We set up a collaboration with Indonesian researchers, including Dr. Alex Masengi, Dr. Renny Hadiaty, Dr. Daniel Mokodongan, Bayu Kreshna Adhitya Sumarto, and their wonderful colleagues. We visited the habitats of Oryzias woworae (Fig. 2). The most brightly red population inhabits a blue light-dominant spring, where the red fins make a good contrast with the blue background (Fig. 3).

Fig. 3. Contrast between red coloration and blue water.

Next, we set up a collaboration with Dr. Atsushi Toyoda, an expert in de novo genome assembly, to make a reference genome sequence of Sulawesian medakas. Dr. Koji Mochida, Dr. Shingo Fujimoto, and their colleagues in Yamahira Lab reared and phenotyped the hybrid fish, followed by genotyping by Satoshi and Dr. Atsushi Nagano. Satoshi found a peak of QTL and identified one strong candidate gene colony stimulating factor 1 (csf1) on an autosome. At first, I was a little bit disappointed because it was not on the sex chromosome, but it was very exciting that we could identify a good candidate gene underlying the evolution of sexual dichromatism. csf1 is known to be involved in pigment cell development in the zebrafish.

After moving to Dr. Kiyoshi Naruse's laboratory, Satoshi applied his expertise in genome editing to Oryzias woworae and found that csf1-knockout fish did not show red coloration. This strongly suggests that this is the causative gene. Then, Satoshi conducted a mate choice experiment to test whether females prefer red males to non-red (knockout) males as the sexual selection theory posits (Fig. 4). The answer was yes. Next, Satoshi conducted a predator attraction experiment. Sexual selection theory often posits that red males attract predators as well. Contrary to this hypothesis, predators were more attracted to non-red (knockout) males. This result seemed puzzling at first. However, we found several previous studies indicating that some predators tend to attack weaker prey because such prey can be more easily caught. If the red coloration signals an escape ability, it is not surprising that the predators choose non-red males. This is still a hypothesis until any experiments prove this hypothesis.

Fig. 4. Red males attract females but not predators.

Our long-term collaboration has demonstrated that integration of genome editing and genome sequencing technologies can identify causative genes underlying sexually selected traits and provide a new avenue for testing theories of sexual selection. There are many other unanswered, but exciting questions. If the red coloration is beneficial for both attracting females and avoiding predators, why don't females show red coloration? Are there any unidentified costs for females becoming red? Another important question is what the causative mutation is. Answering these questions will contribute to a better understanding of the evolutionary mechanisms of sexually dimorphic ornaments.

The “Sex Role” Concept: An Overview and Evaluation

“Sex roles” are intuitively associated to stereotypic female and male sexual strategies and in biology, the term “sex role” often relates to mating competition, mate choice or parental care. “Sex role reversals” imply that the usual typological pattern for a population or species is deviates from a norm, and the meaning of “sex role reversal” thus varies depending upon whatever is the usual pattern of sex-typical behavior in a given taxon. We identify several problems with the current use of the “sex role” concept. (1) It is typological and reflects stereotypic expectations of the sexes. (2) The term “sex role” parses continuous variation into only two categories, often obscuring overlap, between the sexes in behavior and morphology, and variability in relation to ecological circumstances. (3) Common generalizations such as “sex role as seen in nature” mask variation upon which selection may act. (4) The general meaning of “sex roles” in society (i.e. “socially and culturally defined prescriptions and beliefs about the behavior and emotions of men and women”) is contrary to biological “sex role” concepts, so that confusing the two obscure science communication in society. We end by questioning the validity of the “sex role” concept in evolutionary biology and recommend replacing the term “sex role” with operational descriptions.

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Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

Brian A. Lerch & Maria R. Servedio

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B.A.L. conceived of the project and the optimization models. B.A.L. and M.R.S. designed the population genetic models. B.A.L. led the writing on the manuscript with input from M.R.S.

Corresponding author

Materials and Methods

Empirical experiments

We sampled 1330 adult onion thrips (T. tabaci) from 32 onion or leek crop fields in Kuriyama, Naganuma, Nanporo and Kitami city, in Hokkaido prefecture, Japan, from July to September in 2009, 2010 and 2011 (see Supplementary Fig. S5 for a map of the sampling locations). Each crop field was treated as a population. The thrips were dislodged from their host plants onto a white plastic tray by gently shaking the host plant, and then collected using an aspirator. All sampled individuals were sorted into male adult, female adult and larva under a microscope based on the presence or absence of an ovipositor and wings. In the following experiments, we only used adults because the larvae cannot be distinguished their sex. Next, genomic DNA was extracted from the whole body of each the adult using the modified Chelex method 17 . Dried individuals were crushed in 200 μl of a 5% Chelex solution (Bio-Rad, Hercules, CA, USA 10 mM Tris-HCl, pH 8.0) and 5 μl of proteinase K (TaKaRa, Otsu city, Shiga, Japan 20 mg/ml), and then incubated at 55 °C for more than 12 hours in 1.5-ml microcentrifuge tubes. Subsequently, the mixtures were boiled at 98 °C for 10 min to inactivate proteinase K. The template DNA were obtained from the aqueous layer next to the Chelex layer.

The reproductive mode of each adult female was determined via polymerase chain reaction with strain-specific primers 16 . The primer set included one primer that encoded a sequence shared by the strain (TCOR, 5′-attgcgtaaattattcctaaaagtcca-3′) and two primers (sexual strain-specific primer TCOS, 5′-aacagcTattctCcttcttttatctC-3′ asexual strain-specific primer TCOC, 5′-gaacagtatatccacctttatcaacG-3′ the capital letters indicate strain-specific nucleotides) that amplified mtDNA fragments of different lengths corresponding to the reproductive modes (261 bp for the asexual strain and 451 bp for the sexual strain). The composition of reaction mixture used for PCR-SSP was as follows: each 10 μl reaction mixture comprised 5 pmol of the consensus primer, 2.5 pmol of each strain-specific primer, 5 μl 2 × MightyAmp Buffer, 0.1 μl MightyAmp DNA Polymerase (TaKaRa 1.25 U/μl), and 0.5 μl template DNA. PCR-SSP was performed using a 2720 Thermal Cycler (Applied Biosystems, Foster city, CA, USA) with the following temperature cycles: initial denaturation for 2 min at 98 °C, followed by 35 cycles of denaturation and annealing, consisting of 10 sec at 98 °C and 1 min at 60 °C, and a final extension step of 1 min at 68 °C. The fragment lengths of the PCR products were detected via 1% agarose gel electrophoresis using 5 μl of a 100-bp DNA ladder (TaKaRa) with ethidium bromide staining. Then, the sex ratio of each population was calculated by dividing the number of males by the number of sexual individuals, and similarly the sexual:asexual ratio of each population was obtained by dividing the number of sexual individuals by the total number of adults.

After strain identification, up to 20 randomly chosen sexual females were genotyped at nine microsatellite loci to infer phylogenetic relationships among the populations. To amplify these microsatellite loci, a 2720 Thermal Cycler (Applied Biosystems) was used for PCR, which was performed as follows: initial denaturation of 2 min at 96 °C, followed by 35 cycles of denaturation for 5 sec at 98 °C, annealing for 30 sec at temperatures specific to each primer pair, extension for 1 min at 68 °C, and a final extension of 1 min at 68 °C. The primer sequences and annealing temperatures for these microsatellite loci were described previously 23 , in which we confirmed Mendelian inheritance of microsatellite alleles in the sexual strain. Each 10 μl reaction mixture comprised 2 pmol of primers, 5 μl 2 × MightyAmp Buffer, 0.1 μl MightyAmp DNA Polymerase (TaKaRa, Otsu, Japan 1.25 U/μl), and 1 μl template DNA. A 1-μl aliquot of the PCR product was electrophoresed in tandem with 0.5 μl of Size Standard Kit 400 (Beckman-Coulter, Fullerton, CA, USA) in a CEQ-8000 Genetic Analyzer (Beckman-Coulter). Based on the data obtained regarding allele frequencies, the pairwise genetic distances (FST) between the 32 populations and deviations from Hardy-Weinberg equilibrium for each population were calculated using the program Arlequin, version 24 . Then, a neighbor-joining tree was constructed from the pairwise genetic distance matrix using MEGA version 5 software 25 .

Phylogenetically independent contrasts were used to remove the effect of phylogeny from the correlation analysis between the sex ratio and the sexual:asexual ratio. We arranged population pairs without any overlapping branches in the inferred neighbor-joining tree. Thus, 16 population pairs were obtained from the 32 populations (Supplementary Fig. S1). The differences between the sex ratios and the sexual:asexual ratios were calculated for each of the population pairs. This method provides statistically independent values that represent the amount of change on each branch in the phylogeny 22 . Using these differences, we analyzed the evolutionary relationship between the sex ratios and the sexual:asexual ratios.

To explore differences in reproductive rates between the strains, we sampled an additional 50 adult females from each of five crop fields in Nanporo, Hokkaido prefecture, Japan. These females were individually reared in 50-ml centrifuges tubes with 5 ml of molded plaster in a 25 °C chamber under the long-day condition (14 L:10D). A garlic clove with the skin removed was provided for each the female as a food source and oviposition substrate. After 3 days, we removed the adult females from the centrifuge tubes and assessed their reproductive modes using the method described above. The females that died at this point of time were excluded from the following analysis. On the 20th day after the onset of rearing, we sampled and counted all individuals within the centrifuge tubes. At the end of the experiment, we checked the sex of each reproduced adult under a microscope.

All statistics were performed using the computer program R, version 3.1.0. For proportional data (sexual:asexual ratios and sex ratios), we used generalized linear models using the quasi-binomial logit link in the ‘glm’ function and obtained statistical values using the ‘Anova’ function in the ‘car’ package. For the other data (differences in the phylogenetically independent contrast analysis, number of offspring and residuals), we used a general linear model using the ‘lm’ function and the ‘Anova’ function.


To assess the possibility that female-biased sex ratios evolve in sexual populations of T. tabaci to compete with their asexual counterparts, we constructed an individual-based model, assuming a haploid population including sexual males and females and asexual females, with discrete generations in 10,000 patches (subpopulations), where the following events occurred within each generation in the following order: mating, dispersal, pesticide application and reproduction.

Mating occurred randomly among sexual individuals within a patch (the males could mate repeatedly, whereas the sexual females mated just once) and was skipped for asexual females, after which all males died, and the females then either remained in their natal patch or dispersed at a dispersal rate of d, which was genetically determined by a single locus (0 < d < 1). Dispersal was considered successful at a probability of p = 0.02, 0.05 or 0.1, and if it failed, the females died. A destination patch was randomly chosen from all of the patches. After dispersal, a pesticide was applied to all individuals in the patches when the number of individuals was greater than a certain threshold value (t = 10, 20 or 40). Subsequently, asexual females produced genetically identical daughters except for in cases of mutation, whereas sexually produced offspring inherited one allele from either the mother or father at each locus. For sexual reproduction, the sex ratio (proportion of males among the offspring m) was determined according to two strategies: the first was based on LMC theory 21 and was represented as (n−1)/2n (n indicates the number of sexual females in a patch), whereas the second was based on the genetic value of locus g (0 < g < 1). These two strategies of the sexual females were switched by another locus (L = 0 or 1 if the value is zero, the female uses her genetic value, whereas if the value is one, she follows the prediction of the LMC theory). We assumed random mutations at a constant probability per generation per locus (i.e., 0.001). If a mutation occurred, the gene was replaced with a random value between 0 and 1 at the locus corresponding to dispersal rate d and male ratio m, and a value of 0 or 1 was used for the locus corresponding to the switch of sex ratio strategy L. After reproduction, all adults died, and the next generation began.

We started the simulations with 10,000 sexual individuals with random genetic values for all loci. After 1,000 generations, 1,000 asexual individuals were introduced into randomly chosen patches. We assessed the effects of three parameters: (i) the benefit of sexual reproduction based on the number of offspring per female (20 for sexual individuals and 15 or 20 for asexual individuals) (ii) the probability of dispersal success (p = 0.02, 0.05 or 0.1) and (iii) the threshold of pesticide application (t = 10, 20 or 40). For each of the 18 parameter sets, we ran 100 simulations and recorded population dynamics and gene frequencies between reproduction and mating events until either the extinction of sexual or asexual strain occurred, or 10,000 generations had been simulated. We performed all simulations using Visual C++ 2012 and have provided the code for the simulations as a supplementary note online.

The Cost of Biparental Sex Under Individual Selection

Models of evolutionarily stable strategies are presented, which were designed to determine whether the disadvantage of anisogamous biparental sex is due to the cost of male allocation or to the cost of meiosis. The results show that (1) the cost of biparental sex is due to gene sharing given mutations increasing the proportion of non-cleistogamous parthenogenetic ova in cosexual individuals and (2) the cost of biparental sex is due to male allocation given mutations increasing somatic reproduction in cosexual individuals and mutations increasing partial pathenogenesis in dioecious females. It is suggested that, in general, the cost of biparental sex is due to male allocation when mutations that increase uniparental reproduction affect events before the male-allocation decision, and that the cost of biparental sex is due to gene sharing when mutations that increase uniparental reproduction affect events that come after the male-allocation decision.


The defining distinction between males and females is based on investment in the zygote: females provide the bulk of the cytoplasm via a large egg, while males contribute virtually nothing with either a tiny sperm cell or pollen grain. In species with internal fertilisation and/or brood care, this asymmetry in investment can extend to later developmental stages of the offspring, since males often contribute little or nothing. John Maynard-Smith argued that this difference in investment implies that sexual reproduction has a twofold cost compared to asexual [1]. In an outcrossing sexual population, the stable sex ratio is 50:50, so on average individuals ‘waste’ 50% of resources on males who inefficiently convert resources into offspring. A mutation that induces asexuality in a sexual population with two separate sexes would initially double in frequency each generation, since, all else being equal, asexuality is exactly twice as efficient at converting resources into descendants.

A new study in BMC Biology shows that termite species can abandon males altogether, consistent with Maynard-Smith’s idea that asexual variants can gain a short-term benefit over sexual relatives. Queens of some populations of the species Glyptotermes nakajimai reproduce without any genetic contribution by males, not only to produce new queens, but also to produce sterile workers and soldiers [2]. Dissections of more than 4200 individuals, belonging to soldiers, workers and reproductives of 37 colonies from six populations, did not uncover a single male. Colonies of the four other populations of the same species all contained both male and female individuals in roughly equal numbers, for reproductive, worker and soldier castes. In further support of the absence of males, the spermathecae—the storage organs for sperm—of queens of the six all-female populations did not carry any sperm, while spermathecae of queens from the other populations were filled with sperm. The exact mechanism whereby reproduction without fertilization by males occurs is unknown, either by some form of self-fertilisation (automixis, either via gamete duplication or gamete fusion) or purely asexual reproduction (apomixis) where eggs are produced by mitosis. Since the chromosome number of the asexual populations likely is uneven, apomixis is most plausible.

By producing all-female societies, colonies of this termite resemble colonies of Hymenopteran social insects, the ants, social wasps and bees, where sterile helpers are exclusively female. It was long believed that this sex bias is a consequence of their peculiar sex determination. Sex in Hymenoptera is determined by ploidy: unfertilized, haploid, eggs develop into males, while fertilized, diploid, eggs develop into females. Haplo-diploid sex determination has interesting implications for relatedness (r) among different colony members (Fig. 1a). In a colony founded by a single queen mated with a single male, daughters have a relatedness of ¾ with their sisters, since they all have half of their genome in common via the haploid father and additionally on average one quarter via their diploid mother. In contrast, their relatedness to their own offspring is only ½. According to the haplo-diploidy hypothesis, proposed by Bill Hamilton, this difference in relatedness would predispose females to become workers, as they could increase their inclusive fitness more by helping their mother raise sisters to become new queens than by producing new queens themselves [3].

Standard life cycles of ants (a) and termites (b) and deviations due to conflicts between the reproductive interests of queens and males. The genome representation of ancestors is indicated in colours in the offspring (adapted with permission from a sketch made by David Nash). a Ants have a haplo-diploid life cycle, where unfertilized eggs become males and fertilized eggs either workers or female alates. All workers in an ant society are female. In some ants, queens reproduce parthenogenetically to produce alates, but sexually to produce workers, thus parasitizing on males [5]. In yet another deviation, queens and males each produce their own female and male alates via asexual reproduction, but workers via sexual reproduction [6]. Finally, some ant species have become obligately asexual, where both workers and new queens are produced without any contribution of males [7]. b In contrast to ants, termites are diploid social insects. In the ‘standard’ life cycle, a single queen and king found a colony and produce sterile helpers (workers and soldiers) and fertile alates via sexual reproduction. In some species, replacement reproduction occurs, where the primary queen and king can be replaced by their own offspring [8]. In some species the queen can produce a replacement queen by asexual reproduction [9]. Finally, some populations of the species Glyptotermes nakajimai have all-female societies, which form alates and workers via asexual reproduction [2]

However, the flipside of haplo-diploid sex determination is that sisters are less related to their brothers (r = ¼) than to their own sons (r = ½). Later on it was realised that this implies that all-female societies of Hymenoptera cannot be explained by the haplo-diploidy hypothesis, since the average relatedness among females and siblings is ½, exactly equal to relatedness with own offspring. Instead, a recent analysis found support for the hypothesis that the sex of helpers can be explained by variation in the ecological factors that favoured eusociality [4]. According to this idea, if the original task of helpers was to rear brood, we would expect the helpers to be drawn from the sex or sexes that provided parental care in the ancestral non-social species, which is usually females. The original task of helpers in social Hymenoptera was indeed brood rearing. In contrast, in termites it is likely that helpers originally had multiple tasks, including colony defence. Since the ancestors of termites occupied wood trunks that provided their food, they lived inside their food, which constituted a valuable resource worth defending against competitors. Since neither sex is pre-adapted for defensive tasks, we would expect the helpers to be drawn from both sexes. This could explain why helper castes in most termite species usually are a mixture of male and female individuals.

Even though high relatedness among sisters is no longer believed to explain the sex of workers of Hymenopteran species, kin-selection theory does provide the explanation for the evolution of the extreme altruism seen in societies of social insects. By helping their mother produce fertile offspring, sterile individuals can increase their inclusive fitness via the genes present in genetically related individuals. However, differences in relatedness between colony members also provide a rich ground for conflicts between different colony members. Kin conflicts have been studied most extensively in ants (Fig. 1a). Some remarkable outcomes of such conflicts have been described recently. In the ant species Cataglyphis cursor, males and workers are produced via normal sexual reproduction, from unfertilized and fertilized eggs, respectively, but queens clone themselves to produce new queens [5]. Queens thus parasitize on males, since males do not contribute any genetic material to reproductives of the next generation, but only to workers. In other cases, however, the conflict between males and females over transmitting genes has resulted in a draw. In a few ant species, workers are produced sexually, but female and male reproductives asexually. In those cases, it is thought that the males manage to exclude the maternal genome from fertilised eggs, thus clonally propagating themselves [6]. Interestingly, in those cases, males and females represent evolutionarily completely separated lineages whose genomes only come together in the workers. Finally, like the newly discovered termite populations, some ant species have also disposed of males completely, and reproduce asexually [7].

In termites, kin conflicts have been studied less extensively (Fig. 1b). In some species, one or more offspring can replace a primary reproductive that has died and become a replacement or secondary reproductive. Replacement reproduction results in inbreeding and can happen repeatedly in a single colony. This was once believed to be important for the evolution of reproductive altruism in diploid organisms, since inbreeding increases relatedness among colony members [8]. In 2009, Matsuura and co-workers discovered that in some termite species, secondary queens are produced by parthenogenesis of the primary queen, so-called asexual queen succession (AQS) [9]. By cloning herself, the queen can extend her (genetic) lifespan. An additional consequence is that the queen can increase her genetic contribution to offspring beyond the 50% that results from normal reproduction. The reason is that the primary king cannot produce secondary kings by parthenogenetic reproduction, but only by mating with the queen.

The one-sided, mother–son inbreeding which can result from mating between the cloned queen and the secondary king in long-lived colonies implies that colony members are then related by ¾ to the primary queen, and only by ¼ to the primary king [10] (Fig. 2). This implies that, from an inclusive-fitness perspective, female reproductives are more valuable for colony members, both male and female, than male reproductives. Kin-selection theory therefore predicts that workers should favour a female-biased sex ratio of the alates, which is supported by empirical evidence for several species with AQS, and, as expected, not for species without AQS [9]. Here, I want to propose another possible corollary of this difference in relatedness between helpers and the primary king and relatedness between helpers and the primary queen. Since sex determination in termites is chromosomally based on an XY system, random segregation of X and Y chromosomes will lead to an equal sex ratio. However, since caste of an offspring is determined by environmental factors influenced by helpers, helpers can influence the sex ratio of the alates. Since helpers, irrespective of their sex, all have an interest in a more female-biased sex ratio of the alates, a direct consequence of raising more female offspring as alates may be that a larger proportion of the remaining offspring that become helpers are male. A testable prediction, therefore, is that species with AQS, in conjunction with a more female-biased sex ratio of the alates, have a more male-biased sex ratio of the helper castes. Consistent with this prediction, the species Reticulitermes virginicus, which has AQS and the most strongly female-biased alate sex ratios, shows a significantly male-biased worker sex ratio, although the sex ratio of soldiers is female biased (Matsuura, personal communication). Clearly, more research is needed to test this hypothesis.

The consequences of replacement reproduction for relatedness of colony members to the primary queen and king. a ‘Standard’ replacement reproduction, where secondary reproductives are both produced sexually by the primary reproductives. b Replacement reproduction where the secondary queen is formed by asexual queen succession, so that the primary queen extends her genetic life span, but the secondary king is formed by sexual reproduction of the primary king and queen

The increased tendency for the helper castes to become male biased for species with AQS may constrain the evolution of all-female asexual reproduction of such species, since they rely on males as a work force. It therefore may make sense that the all-female societies of G. nakajimai discovered now [2] belong to a family where AQS is not known (Kalotermitidae). It is ironic that in the group where males contribute more to raising the offspring than any other group of social insects, females of some populations have gotten rid of males. Yet, the benefit of saving on the twofold cost of sex remains: since males contribute so little to the zygote, diverting resources away from males towards females can be selected for. In G. nakajimai the more uniform morphology of the soldier caste appears to provide an additional advantage in colony defence, allowing asexual populations to maintain a smaller soldier force [2].

The rarity of purely asexual reproduction and the empirical finding that asexual lineages generally represent terminal branches in the tree of life suggest that asexuality is doomed to death on the long term. Nevertheless, the split between the sampled asexual and sexual lineages in Glyptotermes nakajimai is estimated to have occurred 14 million years ago [2]. However, as acknowledged by the authors, this time estimate may not indicate the split of asexuality from sexual ancestors, but only the maximum divergence time. Finding populations intermediate in divergence from those two clusters of lineages could give a more realistic estimation of the age of asexuality in this termite species. Time will thus have to tell how long these colonies of emancipated females have managed to survive without males.


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“Using Detection Dogs to Conduct Simultaneous Surveys of Northern Spotted (Strix occidentalis caurina) and Barred Owls (Strix varia)“ Samuel K Wasser, Lisa S. Hayward, Jennifer Hartman, Rebecca K. Booth, Kristin Broms, Jodi Berg, Elizabeth Seely, Lyle Lewis, Heath Smith

2012 PLoS ONE, 7(6): e36842

“Distinguishing the Impacts of Inadequate Prey and Vessel Traffic on an Endangered Killer Whale (Orcinus orca) Population“ Katherine L. Ayres, Rebecca K. Booth, Jennifer A. Hempelmann, Kari L. Koski, Candice K. Emmons, Robin W. Baird, Kelley Balcomb-Bartok, M. Bradley Hanson, Michael J. Ford, Samuel K. Wasser

2011 Proceedings of the Royal Society, Biological Sciences

“Evidence that ship noise increases stress in right whales“ Rosalind M. Rolland, SE Parks, KE Hunt, M Castellote, PJ Corkeron, DP Nowacek, SK Wasser and SD Kraus

2011 Frontiers in Ecology and the Environment
2011 General and Comparative Endocrinology, 172: 382-391
2011 Ecosphere, 2(6): 1-20
2011 PLoS One, 6(12): e28939
2010 General and Comparative Endocrinology, 168(1): 1-7

“Non-invasive measurement of thyroid hormone in feces of a diverse array of avian and mammalian species“ SK Wasser, JC Azkarate, RK Booth, L Hayward, K Hunt, K Ayers, C Vynne, K Gobush, D Canales-Espinosa, E Rodriguez-Luna

2010 General and Comparative Endocrinology, 169: 117-122
2010 Endangered Species Research, 11: 69-82

“Species and stock identification of prey consumed by endangered southern resident killer whales in their summer range“ MB Hanson, RW Baird, JKB Ford, J Hempelmann-Halos, DM Van Doornik, JR Candy, CK Emmons, GS Schorr, B Gisborne, KL Ayers, SK Wasser, KC Balcomb, K Balcomb-Bartok, JG Sneva, MJ Ford

2010 Conservation Biology, 25(1): 154-162

“Effectiveness of scat-detection dogs in determining species presence in a tropical savanna landscape“ C Vynne, JR Skalski, RB Machado, MJ Groom, ATA Jacomo, J Marinho-Filho, MB Ramos Neto, C Pomilla, L Silveira, H Smith, SK Wasser

2010 Science, 328: 1633-1635

“Response — Consequences of Legal Ivory Trade“ SK Wasser, K Nowak, J Poole, J Hart, R Beyers, P Lee, K Lindsay, G Brown, P Granli, A Dobson

2010 Science, 327: 1331-1332

“Elephants, Ivory, and Trade“ SK Wasser, J Poole, P Lee, K Lindsay, A Dobson, J Hart, I Douglas-Hamilton, G Wittemeyer, P Granli, B Morgan, J Gunn, S Alberts, R Beyers, P Chiyo, H Croze, R Estes, K Gobush, P Joram, A Kikoti, J Kingdon, L King, D Macdonald, C Moss, B Mutayoba, S Njumbi, P Omondi, K Nowak

2009 Scientific American, 68-76
2009 Journal of Zoo and Wildlife Medicine, 40(2): 382-384
2009 Animal Behaviour, 78: 1079-1086
2009 Journal of Wildlife Management, 73(7): 1233-1240

“Scent Matching Dogs Determine Number of Unique Individuals from Scat” SK Wasser, H Smith, L Madden, N Marks, C Vynne

2009 Molecular Ecology, 18: 722-734

“Genetic Relatedness and Disrupted Social Structure in a Poached Population of African Elephants” KS Gobush, B Kerr, SK Wasser

2009 Conservation Biology, 22: 1590-1599.

“Long-Term Impacts of Poaching on Relatedness, Stress Physiology, and Reproductive Output of Adult Female African Elephants” KS Gobush, BM Mutayoba, SK Wasser

2008 Natural History, pp.48-53

“Lucky dogs: Dogs sniff out scat from endangered animals, trumping more technical tracking methods” SK Wasser

2008 Conservation Biology, 22: 1065-1071
2007 Nature Protocols, 2: 2228-2232

“Isolation of DNA from small amounts of elephant ivory” C. Mailand, SK. Wasser

2007 Proceedings National Academy of Sciences, 104: 4228-4233

“Using DNA to track the origin of the largest ivory seizure since the 1989 trade ban” S Wasser, C Mailand, R Booth, B Mutayoba, E Kisamo, B Clark, M Stevens

2006 Journal of Cetacean Research and Management, 8(2):121-125

“Faecal sampling using detection dogs to study reproduction and health in North Atlantic right whales (Eubalaena glacialis)” R Rolland, P Hamilton, S Kraus, B Davenport, R Gillett, S Wasser

2006 African Journal of Biotechnology, 5: 1588-1593

“The potential of mitochondrial DNA markers and polymerase chain-reaction fragment length polymorphism for domestic and wild species identification” A Malisa, P Gwakisa, S Balthazary, S Wasser, B Mutayoba

2006 General and Comparative Endocrinology, 148: 260-272
2005 African Journal of Biotechnology, 4: 1269-1274
2005 Zoo Biology, 24: 403-417

“Longitudinal monitoring of fecal testosterone in male Malayan sun bears (Ursus malaynus)” H Hesterman, SK Wasser, JF Cockrem

2005 Annals of the New York Academy of Sciences, 1046: 109-137

“Noninvasive measures of reproductive function and disturbance in the barred owl, great horned owl, and northern spotted owl” SK Wasser, KE Hunt

2005 General and Comparative Endocrinology, 142: 308-317

“Assessing reproductive status of right whales (Eubalaena glacialis) using fecal hormone metabolites” RM Rolland, KE Hunt, SD Kraus, SK Wasser

2004 Proceedings National Academy of Sciences, 101: 14847-14852

“Assigning African elephant DNA to geographic region of origin. Applications to the ivory trade” SK Wasser, A. Shedlock, K. Comstock, E. Ostrander, B. Mutayoba, M. Stephens.

2004 Behavioral Ecology and Sociobiology, 56: 328-337

“Infant handling and mortality in yellow baboons (Papio cynocephalus): evidence for female reproductive competition?” S Kleindorfer, SK Wasser

2004 Behavioral Ecology and Sociobiology, 56: 338-345.

“Population trend alters the effects of maternal dominance rank on lifetime reproductive success in yellow baboons (Papio cynocephalus)” SK Wasser, GW Norton, S Kleindorfer, RJ Rhine

2004 Canadian Journal of Zoology, 82: 475-492
2004 Physiological and Biochemical Zoology, (in press)

“Factors Associated With Fecal Glucocorticoids In Alaskan Brown Bears (Ursus arctos horribilis)” CG van der Ohe, SK Wasser, K. Hunt, C Servheen

2004 Physiology and Behavior, 80: 595-601

“Validation of a fecal glucocorticoid assay for Steller sea lions (Eumetopias jubatus)” KE Hunt, A Trites, SK Wasser

2003 Physiological and Biochemical Zoology, 76: 918-928

“Effect of long-term preservation methods on fecal glucocorticoid concentrations of grizzly bear and African elephant” KE Hunt, SK Wasser

2003 General and Comparative Endocrinology, 134: 18-25

“Noninvasive reproductive steroid hormone estimates from fecal samples of captive female sea otters (Enhydra lutris)” S Larson, CJ Casson, SK Wasser

2003 Conservation Biology, 17: 1-4

“Amplifying nuclear and mitochondrial DNA from African Elephant Ivory: A tool for monitoring the ivory trade” KE Comstock, EA Ostrander, SK Wasser

2002 Molecular Ecology, 11:2489-2498

“Patterns of molecular genetic variation among African elephant populations” KE Comstock, N Georgiadis, J Pecon-Slattery, AL Rocca, SJ O’Brien, SK Wasser

2002 Conservation Genetics, 3: 435-440

“An evaluation of long-term preservation methods for brown bear (Ursus arctos) faecal DNA samples” MA Murphy, LP Waits, KC Kendall, SK Wasser, JA Higbee, R Bogden

2002 Conservation Medicine: Ecological Health in Practice, pp 130-144

“Assessing stress and population genetics through non-invasive means” Aguire, AA., RS Ostfeld, GM Taber, C House, MC Pearl (eds.) SK Wasser, KE Hunt, CM Clarke

2001 Wildlife Society Bulletin, 29: 899-907

“Fecal glucocorticoid assays and the physiological stress response in elk” JJ Millspaugh, RJ Woods, KE Hunt, KJ Raedeke, GC Brundige, BE Washburn, SK Wasser

2001 Reproductive Ecology and Human Evolution, pp. 137-158

“Reproductive filtering and the social environment” SK Wasser and N. Place

2001 Western Black Bear Workshop, 7: 24-29

“Technical considerations for hair genotyping methods in black bears” CM Clarke, DA Immell, SK Wasser

2001 Ursus, 12: 237-240

“Fecal DNA methods for differentiating grizzly bears from black bears” CM Clarke, JA Fangman, SK Wasser

2001 Conservation Biology, 15: 1134-1142

“Non-invasive stress and reproductive measures of social and ecological pressures in free-ranging African elephants (Loxodonta africana)” CAH Foley, S Papageorge, SK Wasser

2000 General and Comparative Endocrinology, 120: 260-275

“A generalized fecal glucocorticoid assay for use in a diverse array of non-domestic mammalian and avian species” SK Wasser, KE Hunt, JL Brown, K Cooper, CM Crockett, U Bechert, JJ Millspaugh, S Larson, SL Monfort

2000 Molecualr Ecology, 9: 993-1011

“Polymorphic microsatellite DNA loci identified in the African elephant (Loxodona africana)” KE Comstock, SK Wasser, EA Ostrander

2000 American Journal of Primatology, 51: 229-241

“Lifetime reproductive success, longevity, and reproductive life history of yellow baboons (Papio cynocephalus) of Mikumi National Park, Tanzania” RJ Rhine, G Norton, SK Wasser

1999 General and Comparative Endocrinology, 114: 269-278

“Serum prolactin concentrations in the captive female African elephant (Loxodonta africana): Potential effects of season and steroid hormone interactions” U.S. Bechert, L. Swanson, SK Wasser, D.L. Hess, F. Strormshak

1999 American Journal of Obstetrics and Gynecology, 180: S272-274

“Stress and Reproductive Failure: An Evolutionary Approach with Applications to Premature Labor” SK Wasser


As explained before, the four SR populations have a strong female bias. If Fisher's Principle really works, it will select for the autosomal suppressors and gradually restore equal sex proportions. Only the autosomes are genetically variable so, barring mutation, sex chromosomes could not cause changes in the sexual proportion. The SR populations carry a X-Y meiotic drive system but this does not violate the Fisher's Principle assumption of Mendelian segregation of the alleles controlling the sexual proportion: the control was effectively autosomal, for the SR and Y chromosomes were fixed. The control was also parental (and not zygotic): the autosomal suppressors are expressed in the parental males.

Now suppose that we do observe an increase in the male proportion. A general and robust demonstration of Fisher's Principle would require testing three critical predictions: (i) there must be enough autosomal genetic variation in the sexual proportion to account for its observed rate of change (ii) this change should have been caused by the increase in the frequency of the autosomal alleles that direct the reproduction to the rare sex, the males (iii) female excess, rather than pleiotropic fitness effects, should have caused the spread of these alleles. These tests guard us against “mimic” evolutionary forces, such as sex chromosome effects and natural selection unrelated to Fisher's Principle. Prediction (i) was tested by estimating the realized heritability of the sexual proportion. If Fisher's Principle was the cause of the increase of male proportion, then a direct measurement of h 2 in the same populations (e.g., by father-offspring regression V arandas et al. 1997) should produce a compatible value.

The ST populations allowed the test of predictions (ii) and (iii): as these populations could not have suffered the Fisherian selection (because they lack the female excess), their autosomes were nearly equivalent to a “sample” of the autosomes from the SR populations at generation 0. By comparison between the autosomes from the ST and SR populations at the end of the experiment, we could verify whether SR populations accumulated autosomal suppressors (prediction ii). At the same time, possible pleiotropic fitness effects (of the autosomal suppressors) unrelated to Fisher's Principle were automatically discounted (prediction iii) because they should affect SR and ST populations equally. Thus, if these two Fisher's Principle predictions hold true for our experimental system, then the autosomes of the SR populations should have more suppressor alleles than the autosomes from the ST populations. This comparison was carried out as described before (Figure 1): the autosomes from the four SR and the two ST populations were introgressed into a reference SR strain the resulting SR/Y males were crossed and their progenies were counted.

Finally, mutation might have introduced Y variation and caused artifacts. This possibility was tested with populations 7 and 8 (see results ).

Evolution of the sexual proportion in the four SR populations. (A) Populations 1–4. The linear regression is shown. (B) Each point is the average of the four populations. The line is the best fit Fisherian trajectory (Equation 1 parameters: M0 = 0.164 Vp h 2 = 0.00466).

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