Polygynandrous Mating System Research Articles

Large, overlapping home ranges reveal male mating strategies in polygynandrous Eclectus parrots

ABSTRACT The distribution of the resources needed by females for reproduction affects their dispersion in space and time, which in turn influences the number of females a male can defend. When males provide parental care they in turn become a resource for females, and influence where females choose to breed. Combined, these factors explain a preponderance of monogamous and (to a lesser extent) polygynous mating systems in birds. However, less frequently observed mating systems in birds remain harder to explain. Here, we analyse the home ranges of male Eclectus parrots (Eclectus roratus) to investigate how their use of space facilitates an unusual polygynandrous mating system (where multiple males mate with multiple females). Female Eclectus parrots in the rainforests of northern Queensland, Australia, have limited movements. They remain at their nest trees for most of the year and rely on multiple wide-ranging males to bring them their food. We used light aircraft and VHF transmitters to track the movements of four male Eclectus parrots during the breeding season. We combined data on home range size with molecular analyses of a larger sample of breeding birds. Our analyses demonstrate that male home ranges overlap with each other and encompass multiple (3–14) trees with nesting females. We show that some males divide their time between, and gain reproductive success with, females up to 7 km apart. Our tracking and molecular data offer insights into how polygynandrous mating systems relate to space use among males and females.

Reproductive phenology and behaviour of endangered redside dace (Clinostomus elongatus) in urban streams.

Investigation of the reproductive phenology and spawning behaviour of imperilled species in relation to environmental variability is needed to understand a critical component of species life history. In this study, we used redside dace (Clinostomus elongatus), a freshwater leuciscid listed as Endangered under Canada's Species at Risk Act, to model spawning phenology and make predictions about spawning initiation using historical and climate change projected thermal cues (measured as cumulative growing degree days), and provide an ethological description of spawning behaviour. Logistic regression models applied to 4 years of average daily stream water temperature data and field behavioural observations of the onset of spawning activity indicated a 50% probability of spawning initiation when cumulative growing degree days reached 214°C days and a 95% probability of spawning initiation at 288°C days. Using two climate change scenarios (i.e., a mid-century 1.6°C increase and an end of century 3.6°C increase), spawning initiation was predicted to advance 3 days by the year 2050 and 7 days by the year 2100. Underwater video cameras placed at two sites within an urban stream captured 73 unique spawning events revealing that redside dace spawn in pairs as well as in dense, tightly packed groups (more than 20 individuals). Moreover, there is evidence of redside dace having a polygynandrous mating system, as female redside dace spawned with multiple males in 45.2% of the total spawning events recorded. Taken together, this study provides important insights into redside dace spawning initiation and behaviour, key life-history traits having conservation implications for future reproductive success and, ultimately, population dynamics.

Polygynandry and high genetic diversity supported by kinship and population genetics from neotropical catfish ichthyoplankton

AbstractKnowledge about reproductive biology is critical for understanding species ecology and evolution, hence their conservation. However, such information remains elusive for many species due to the difficulty of observing mating in nature. Herein, we coupled population and sociogenetic analysis to assess the reproductive biology of an important South American catfish, the “painted catfish” Pimelodus maculatus. We analysed the genetic diversity and kinship patterns of three wild ichthyoplankton samples identified by DNA barcoding and screened with microsatellite loci. We found the same trend in the three samples analysed: a high number unrelated larvae (r < 0.25) and potential parents involved (Ca1, 24♀:24♂; Ca2, 21♀:23♂; Cin, 24♀:25♂), as well as a high number of familial clusters (ML: 19‐21; MCMC: 23‐26). The data indicate a parental sexual proportion close to 1:1 and a polygynandrous mating system. We found high levels of genetic diversity, low GST values (GST < 0.014), but moderate DEST values between the tributary and reservoir samples (DEST > 0.25; Cin x Ca1 or Cin x Ca2), a similar pattern to the observed in adult populations. These results indicate that the mating system of P. maculatus has played an important role in minimising the loss of genetic diversity, a condition that may have favoured the species in a highly fragmented landscape.

Comparison of Prostate‐Specific Transglutaminase Function in the Great Apes

The copulatory plug is a hardened structure formed through semen coagulation post‐ejaculation which is theorized to protect against remating, stimulate the female reproductive tract, and aid in sperm release and transport. This structure is prevalent in species that experience high levels of sperm competition including chimpanzees and several other primates. Chimpanzees experience high levels of sperm competition due to their polygynandrous mating system. In polygynandry females will mate with multiple partners during an estrus cycle leading to direct competition between the sperm of each male to fertilize the same egg. This varies distinctly from polygynous and monogamous species, such as humans, where females mate with only one male and sperm competition is diminished. Based on previous work in rats, prostate‐specific transglutaminase 4 (TGM4) is implicated as the driving force of the formation of the copulatory plug. TGM4 is a member of the transglutaminase family of enzymes which catalyze the calcium‐dependent formation of an isopeptide bond between glutamine and lysine residues. While humans do not experience a great deal of sperm competition or form a copulatory plug, human semen goes through a similar process of post‐ejaculatory coagulation which is predicted to be carried out by TGM4 under the same mechanism. Interestingly, there are only seven amino acid differences between the human and chimpanzee TGM4s and yet the degree of coagulation between the two species is vastly different. The aim of this study to characterize and compare the function of these proteins to determine the major contributing factor in semen coagulation. The primary hypothesis was that chimpanzee TGM4 would have higher enzymatic activity and more readily cross‐link artificial substrates than human TGM4. To test this hypothesis, the coding sequences were acquired for human and chimpanzee TGM4 as well as eight other primate species. Using a maximum likelihood‐based method, we generated a gene tree of primate TGM4 and calculated dN/dS ratios for each branch. Human TGM4 had a dN/dS ratio of 1.04 suggesting neutral evolution while chimpanzee TGM4 had a ratio of >1 suggesting strong positive selection. We further predicted the sequence of TGM4 of the last human‐chimp ancestor using ancestral sequence reconstruction which utilizes the known phylogenetic tree and a maximum likelihood approach with the software package Phylogenetic Analysis by Maximum Likelihood (PAML). Coding sequences representing TGM4 from humans, chimpanzees, and the last human‐chimp ancestor were cloned into a mammalian expression vector containing a C‐terminal His6tag and were transfected into HEK‐293T cells. Purified TGM4 was used in an in‐vitro colorimetric enzymatic assay to quantify enzymatic activity. Our results suggest that mating system variation has led to differences in both sequence and function of seminal proteins. These functional differences speak to the impact of even a small number of mutations on protein function as well as the influence of environmental pressures on protein evolution.

The ontogeny of sexual dimorphism in free-ranging rhesus macaques.

Reconstructing the social lives of extinct primates is possible only through an understanding of the interplay between morphology, sexual selection pressures, and social behavior in extant species. Somatic sexual dimorphism is an important variable in primate evolution, in part because of the clear relationship between the strength and mechanisms of sexual selection and the degree of dimorphism. Here, we examine body size dimorphism across ontogeny in male and female rhesus macaques to assess whether it is primarily achieved via bimaturism as predicted by a polygynandrous mating system, faster male growth indicating polygyny, or both. We measured body mass in a cross-sectional sample of 364 free-ranging rhesus macaques from Cayo Santiago, Puerto Rico to investigate size dimorphism: 1) across the lifespan; and 2) as an outcome of sex-specific growth strategies, including: a) age of maturation; b) growth rate; and c) total growth duration, using regression models fit to sex-specific developmental curves. Significant body size dimorphism was observed by prime reproductive age with males 1.51 times the size of females. Larger male size resulted from a later age of maturation (males: 6.8-7.8 years versus females: 5.5-6.5 years; logistic model) and elevated growth velocity through the pre-prime period (LOESS model). Though males grew to larger sizes overall, females maintained adult size for longer before senescence (quadratic model). The ontogeny of size dimorphism in rhesus macaques is achieved by bimaturism and a faster male growth rate. Our results provide new data for understanding the development and complexities of primate dimorphism.

Mating systems and predictors of relative reproductive success in a Cutthroat Trout subspecies of conservation concern.

Mating systems and patterns of reproductive success in fishes play an important role in ecology and evolution. While information on the reproductive ecology of many anadromous salmonids (Oncorhynchus spp.) is well detailed, there is less information for nonanadromous species including the Yellowstone Cutthroat Trout (O. clarkii bouvieri), a subspecies of recreational angling importance and conservation concern. Using data from a parentage‐based tagging study, we described the genetic mating system of a migratory population of Yellowstone Cutthroat Trout, tested for evidence of sexual selection, and identified predictors of mating and reproductive success. The standardized variance in mating success (i.e., opportunity for sexual selection) was significantly greater for males relative to females, and while the relationship between mating success and reproductive success (i.e., Bateman gradient) was significantly positive for both sexes, a greater proportion of reproductive success was explained by mating success for males (r 2 = 0.80) than females (r 2 = 0.59). Overall, the population displayed a polygynandrous mating system, whereby both sexes experienced variation in mating success due to multiple mating, and sexual selection was variable across sexes. Tests for evidence of sexual selection indicated the interaction between mating success and total length best‐predicted relative reproductive success. We failed to detect a signal of inbreeding avoidance among breeding adults, but the group of parents that produced progeny were on average slightly less related than adults that did not produce progeny. Lastly, we estimated the effective number of breeders (N b) and effective population size (N e) and identified while N b was lower than N e, both are sufficiently high to suggest Yellowstone Cutthroat Trout in Burns Creek represent a genetically stable and diverse population.

Genomic signatures of divergent selection are associated with social behaviour for spinner dolphin ecotypes.

Understanding the genomic basis of adaptation is critical for understanding evolutionary processes and predicting how species will respond to environmental change. Spinner dolphins in the eastern tropical Pacific (ETP) present a unique system for studying adaptation. Within this large geographical region are four spinner dolphin ecotypes with weak neutral genetic divergence and no obvious barriers to gene flow, but strong spatial variation in morphology, behaviour and habitat. These ecotypes have large population sizes, which could reduce the effects of drift and facilitate selection. To identify genomic regions putatively under divergent selective pressures between ecotypes, we used genome scans with 8994 RADseq single nucleotide polymorphisms (SNPs) to identify population differentiation outliers and genotype-environment association outliers. Gene ontology enrichment analyses indicated that outlier SNPs from both types of analyses were associated with multiple genes involved in social behaviour and hippocampus development, including 15 genes associated with the human social disorder autism. Evidence for divergent selection on social behaviour is supported by previous evidence that these spinner dolphin ecotypes differ in mating systems and associated social behaviours. In particular, three of the ETP ecotypes probably have a polygynous mating system characterized by strong premating competition among males, whereas the fourth ecotype probably has a polygynandrous mating system characterized by strong postmating competition such as sperm competition. Our results provide evidence that selection for social behaviour may be an evolutionary force driving diversification of spinner dolphins in the ETP, potentially as a result of divergent sexual selection associated with different mating systems. Future studies should further investigate the potential adaptive role of the candidate genes identified here, and could probably find further signatures of selection using whole genome sequence data.

Mating System, Reproductive Success, and Sexual Selection in Bluntnose Klipfishes (Clinus cottoides).

A critical part of the sexual selection process in animals is the genetic mating system. Quantifying mating systems, especially in species with cryptic life histories can be challenging. One approach is to use genotypic markers and accurate parentage analysis, along with methods to account for bias when sampling natural populations, to calculate sexual selection metrics derived from Bateman's principles. In this study, 3 microsatellites were used to genotype 48 adults (23 female and 25 male) and 342 offspring from known mothers of live-bearing bluntnose klipfish. Parentage analysis was performed to interpret mating and reproductive success for both sexes. Metrics quantified were the opportunity for selection (I), the opportunity for sexual selection (Is), absolute (βss), and standardized (β'ss) Bateman gradients and the maximum intensity of precopulatory sexual selection (s'max). Multiple mating by both sexes were revealed by parentage analysis. However, females did not show significant Bateman gradients or a significant maximum intensity of precopulatory sexual selection (s'max), whereas male sexual selection metrics were all significantly greater than 0. These results suggest a polygynandrous mating system for this species. There is an opportunity for sexual selection to act on males but not females in this population, which is evolutionary tied to anisogamy, parental investment, and sex roles.

Population distribution, host-switching, and chemical sensing in the symbiotic shrimp Lysmata pederseni: implications for its mating system in a changing reef seascape

Lysmata pederseni, a protandric simultaneously hermaphroditic shrimp that inhabits the tube sponge Callyspongia vaginalis, is monogamous in the central and southeastern Caribbean Sea. We tested the null hypothesis of monogamy in a northern Caribbean population. In the Florida Keys, shrimps did not inhabit host individuals in pairs with a frequency greater than expected by chance alone. Hermaphrodites inhabited sponges solitarily and often brooded embryos. Hermaphrodites do not store sperm and need to be inseminated shortly after molting to fertilize a new batch of eggs. Thus, males and/or other hermaphrodites are likely switching among host individuals in search of sexual partners. Field experiments demonstrated low shrimp host fidelity. Host residence time was ~2 times shorter for males than for hermaphrodites. We inferred a polygynandrous mating system in L. pederseni from the Florida Keys, with male-role and young hermaphrodites often moving among sponges in search of older, more sedentary, female-role hermaphrodites. We expected shrimps to use water-borne chemical cues originating from conspecifics or sponges to locate sexual partners. Experiments demonstrated that shrimps were attracted to water-borne cues originating from sponges but not conspecifics. We have described the mating system of a reef-associated shrimp in a fast-pace shifting seascape increasingly dominated by sponges and vanishing stony corals. In the central and southeastern Caribbean Sea, with greater coral cover and lower sponge abundance than in the Florida Keys, the same species is monogamous. Whether or not similar shifts in the social organization of other coral reef-dwelling marine organisms are occurring due to contemporary changes in seascapes is a relevant topic that deserves further attention.

Individual, social, and sexual niche traits affect copulation success in a polygynandrous mating system

In polygynandrous mating systems, the factors that mediate copulation success and the use of alternative mating tactics, such as mate guarding, are still poorly understood. In the rock hyrax (Procavia capensis), both sexes mate annually with multiple partners during a single month. In order to examine the factors that drive copulation success, we used 494 mating-related observations that were collected over a decade. In our analysis, we used the traits of individual hyraxes as well as the traits of members of their sexual niche, which we defined as their local competitors and potential mates. Using individual traits, we found that overall, female hyraxes rejected copulation attempts more frequently than males, supporting predictions from sexual selection theory. Females who had been mothers in previous years were mate-guarded more by resident males. When we considered the traits of competitors and potential mates in individuals’ sexual niche, we found that when resident males had higher-ranking competitors, their copulation success decreased, irrespective of their own traits. Bachelor male copulation success was not influenced by their competitor’s social status. Female copulation success was positively affected by maternal status and by social network position. Females that were central in the social network and those that had central female competitors had higher copulation success, supporting the benefits of social cohesion and the importance of the social niche. Thus, our results suggest that in polygynandrous mating systems, copulation success is determined not only by individual quality but also by the social and sexual niches that the individual occupies. Social networks describe with whom individuals consort. The complex patterns of sexual relationships in animal societies can also be expressed as networks of mating-related interactions. During our long-term study on the dynamic social relationships of wild rock hyraxes, we observed complex sexual interactions. Our results show that hyraxes choose mating partners from their available mate pool (or sexual niche) taking into account the traits of their actual mates, other potential mates, and those of their competitors. These findings suggest that the sexual niche, describing the subset of available mating partners, is important for mate choice, with significant implications to the study of sexual selection.

She gets many and she chooses the best: polygynandry inSalamandrina perspicillata(Amphibia: Salamandridae)

Polyandry is a widespread mating strategy, found in a broad number of taxa. Among amphibians, polyandry, and multiple paternity as its direct consequence, is quite common in salamanders, especially within Ambystomatidae and Plethodontidae. In the suborder Salamadroidea the existence of two different types of spermatheca allows several kinds of polyandry strategies to appear. We used multilocus microsatellite genotyping to investigate the presence of polyandry and its effects on the paternity in a previously unstudied species with a terrestrial habit, Salamandrina perspicillata. We collected gravid females in their natural habitat and analysed the paternity of the offspring by using the software COLONY and GERUD. We found that all the analysed clutches had been fertilized by 2–4 males and that in every clutch one male had sired most of the offspring. Our results confirmed that polyandry is an important component of the mating system of this species, suggesting that females are able to recognize the sperm of the male that will provide a genetic benefit for their offspring. We found evidence of female cryptic choice based on males' genetic dissimilarity: (1) males who sire most of the offspring of a given female tend to be genetically different from their sexual partner; (2) a same male, when mated with two females, sired a proportion of the offspring inversely correlated with his genetic similarity to the female; (3) genetic dissimilarity between mating partners is positively correlated with offspring heterozygosity. According to the genetic compatibility model, we hypothesized that in the observed non resource-based mating system the indirect benefit for the offspring should reflect interactions between paternal and maternal genomes rather than the inheritance of the so-called ‘good genes’. This study suggests a polygynandrous mating system for the study species and provides the first report in a salamandrid species in natural condition that reproductive success of males is correlated with genetic dissimilarity between mates. Moreover, we found evidence of an offspring benefit (higher heterozygosity) derived from the most genetically dissimilar father.

The largest relative testis size among primates and aseasonal reproduction in a nocturnal lemur, Mirza zaza.

Testis size is an indirect indicator of a species' mating system, along with sexual size and canine dimorphism, existence and usage of mating and advertisement calls as well as the spatial distribution of males and females ready to mate in solitary species. Upon its recent discovery, the northern giant mouse lemur Mirza zaza was suggested to have a polygynandrous mating system and to exhibit seasonal breeding. We tested these predictions in a field study in Sahamalaza National Park, NW Madagascar. We caught 12 M. zaza, before and during the suggested mating period and obtained standard field morphometric measurements, including testes size. We show that M. zaza has the highest relative testis volume among primates, indicating strong sperm competition and polygynandrous mating. In addition, based on inferred age of captured animals, observed mating behavior, a female caught in met-estrus and data from captivity, we suggest M. zaza to be one of the few lemurs that breed aseasonally. Future field work on this endangered species is required to illuminate the causes and consequences of intense promiscuity and aseasonal breeding despite strong habitat seasonality, which distinguish M. zaza from most other nocturnal lemurs.

Multiple mating and reproductive skew in parental and introgressed females of the live-bearing fish Xiphophorus birchmanni.

Just as mating patterns can promote speciation or hybridization, the presence of hybridization can shape mating patterns within a population. In this study, we characterized patterns of multiple mating and reproductive skew in a naturally hybridizing swordtail fish species, Xiphophorus birchmanni. We quantified multiple mating using microsatellite markers to genotype embryos from 43 females collected from 2 wild populations. We also used a suite of single-nucleotide polymorphism markers to categorize females and their inferred mates as either parental X. birchmanni or as introgressed individuals, which carried alleles from a sister species, X. malinche. We found that parental and introgressed X. birchmanni females mated multiply with both parental and introgressed males. We found no difference in mating patterns or reproductive skew between parental and introgressed X. birchmanni females. However, nonintrogressed X. birchmanni males mated more often with large, fecund females. These females also had the greatest levels of skew in fertilization success of males. Thus, our results show that X. birchmanni has a polygynandrous mating system and that introgression of X. malinche alleles has only subtle effects on mating patterns in this species.

No evidence for size‐assortative mating in the wild despite mutual mate choice in sex‐role‐reversed pipefishes

Size-assortative mating is a nonrandom association of body size between members of mating pairs and is expected to be common in species with mutual preferences for body size. In this study, we investigated whether there is direct evidence for size-assortative mating in two species of pipefishes, Syngnathus floridae and S. typhle, that share the characteristics of male pregnancy, sex-role reversal, and a polygynandrous mating system. We take advantage of microsatellite-based “genetic-capture” techniques to match wild-caught females with female genotypes reconstructed from broods of pregnant males and use these data to explore patterns of size-assortative mating in these species. We also develop a simulation model to explore how positive, negative, and antagonistic preferences of each sex for body size affect size-assortative mating. Contrary to expectations, we were unable to find any evidence of size-assortative mating in either species at different geographic locations or at different sampling times. Furthermore, two traits that potentially confer a fitness advantage in terms of reproductive success, female mating order and number of eggs transferred per female, do not affect pairing patterns in the wild. Results from model simulations demonstrate that strong mating preferences are unlikely to explain the observed patterns of mating in the studied populations. Our study shows that individual mating preferences, as ascertained by laboratory-based mating trials, can be decoupled from realized patterns of mating in the wild, and therefore, field studies are also necessary to determine actual patterns of mate choice in nature. We conclude that this disconnect between preferences and assortative mating is likely due to ecological constraints and multiple mating that may limit mate choice in natural populations.

Genetic Evidence for Polygynandry in the Black-Striped Pipefish Syngnathus abaster: A Microsatellite-Based Parentage Analysis

Sexual selection theory predicts that, in organisms with reversed sex roles, more polyandrous species exhibit higher levels of sexual dimorphism. In the family Syngnathidae (pipefish, seahorses, and seadragons), males provide all parental care by carrying developing embryos on their ventral surfaces, and females develop secondary sex characters. Syngnathids exhibit a variety of genetic mating patterns, making them an ideal group to test predictions of sexual selection theory. Here, we describe the mating system of the black-striped pipefish Syngnathus abaster, using 4 highly variable microsatellites to analyze parentage of 102 embryos. Results revealed that 1) both sexes mate multiple times over the course of a pregnancy (polygynandrous mating system), 2) eggs are spatially segregated by maternity within each brood pouch, and 3) larger females have higher mating success (Kolmogorov-Smirnov test; P < 0.05). Together with similar studies of other syngnathid species, our results support the hypothesis that the mating system is related to the intensity of sexual dimorphism.

Male and female reproductive strategies and multiple paternity in the polygynandrous Alpine Accentor Prunella collaris

Five breeding groups of the Alpine Accentor were studied in a Swiss alpine region. The studied groups showed a polygynandrous mating system and each group was formed of 1–4 females and 3–5 males. The females had exclusive territories, while the males cooperated in defending their group territory. Among the males of one group, a linear dominance relationship was usually well established among the alpha, beta and subordinate male S 1. Both frequent copulation and mate guarding strategies were applied. Females advertised their fertility, solicited most of the copulations and mated multiple times with several males. With approximately 350 matings during the short fertile period of 10 days, the Alpine Accentor is one of the bird species with the highest copulation frequency. Intensity of mate guarding and copulation frequency were highest starting 1 day before egg-laying and throughout the egg-laying period. The alpha male guarded a fertile female closely during the ovulation period, while the beta and other subordinate males (S 1, S 2 and S 3) were restricted in their access to fertile females by the alpha male’s mate guarding ability. In most cases, they did not guard mates and solely performed the frequent copulation strategy. Accordingly, higher ranking males got more solicitations from females, maintained a higher copulation frequency, but also refused a greater portion of all mating offers. Sperm competition was intense with 81.8 % of the broods having multiple paternity. The share of matings during the ovulation period best reflected the achieved share of paternity. Alpha, beta and S 1 sired most of the young, while S 2, S 3 and extra-group males were seldom fathers of offspring. At one nest, up to 4 males helped to feed the young, however, usually at a low rate and the overall male help (28 %) was smaller than the female contribution (72 %). In this polygynandrous mating system, females of the studied population lacked full male help but might have benefited from the greater genetic variation of their young, while males have a large individual variance in their lifetime reproductive success with higher ranking males raising their fitness to above average.

Host-use pattern and sexual dimorphism reveals the mating system of the symbiotic pea crabAustinixa aidae(Crustacea: Brachyura: Pinnotheridae)

Austinixa aidaeinhabits burrows of the ghost shrimpCallichirus majorat Perequê-açu beach, Ubatuba, Brazil. We described the host-use pattern and sexual dimorphism ofA. aidaeto test for monogamy given the generality of this mating system in the subfamily Pinnothereliinae (family Pinnotheridae) to whichA. aidaebelongs. Against expectations,A. aidaelives as solitary individuals within burrows more frequently than expected by chance alone. Additional observations suggested thatA. aidaeexhibits a polygynandrous mating system with males moving among burrows in search of receptive females. First, only 21% of the burrows harboured heterosexual pairs of crabs and the body size of paired crabs was poorly correlated. This suggests pair instability and frequent shifts among burrows by male and/or female crabs, as reported before for other symbiotic crustaceans in which the body size of paired crabs is poorly correlated. Second, males paired with females that were sexually receptive (without embryos) or that have been receptive recently (carrying early embryos) were found more frequently than expected by chance alone. The above agrees with that reported for species in which sexual pairing does not last long. Third, sexual dimorphism in terms of claw size and coloration was evident. Claws were larger in males than in females, a condition that argues in favour of male–male competition inA. aidae. In addition, the body coloration of males was more similar to the sand grains of the beach than that of females. This sex-specific coloration suggests that males are ‘better adapted' than females to roam on the surface of the beach in search of burrows because their coloration should diminish the risk of detection by predators. Experiments are needed to reveal the details of the polygynandrous mating system herein inferred forA. aidaeand to understand those conditions favouring particular reproductive strategies in symbiotic decapod crustaceans.

Variation in reproductive success of male and female Columbian ground squirrels (Urocitellus columbianus)

The imbalanced reproductive success of polygynous mammals results in sexual selection on male traits like body size. Males and females might have more balanced reproductive success under polygynandry, where both sexes mate multiply. Using 4 years of microsatellite DNA analyses of paternity and known maternity, we investigated variation in reproductive success of Columbian ground squirrels, Urocitellus columbianus (Ord, 1815); a species with multiple mating by both sexes and multiple paternity of litters. We asked whether male reproductive success was more variable than that of females under this mating system. The overall percentage of confirmed paternity was 61.4% of 339 offspring. The mean rate of multiple paternity in litters with known fathers was 72.4% (n = 29 litters). Estimated mean reproductive success of males (10.27 offspring) was about thrice that of females (3.11 offspring). Even after this difference was taken into account statistically, males were about three times as variable in reproductive success as females (coefficients of variation = 77.84% and 26.74%, respectively). The Bateman gradient (regression slope of offspring production on number of successful mates) was significantly greater for males (βM = 1.44) than females (βF = 0.28). Thus, under a polygynandrous mating system, males exhibited greater variation in reproductive success than females.

Polygynandry and even-sexed dispersal in a population of collared pikas, Ochotona collaris

Sex-biased dispersal is common in mammals, and in most species, the majority of dispersers are juvenile males. However, which sex typically disperses in a species will ultimately be determined by the costs and benefits of dispersal for each sex. These are partly determined by a species’ mating system, with female-defence polygyny being strongly associated with male-biased dispersal. The few mammal species without sex-biased dispersal have been predicted to have a monogamous or polygynandrous mating system and levels of intraspecific competition that affect males and females equally. North American pikas may meet these criteria. Using microsatellite data from a decade of population monitoring, we examined the mating system and dispersal habits of the collared pika, Ochotona collaris, an asocial alpine-dwelling lagomorph. While their behaviour suggests they are monogamous or polygynous, parentage analyses revealed that the pikas were primarily polygynandrous. As predicted, there was no difference in the average distance dispersed by the two sexes, most likely because the costs and benefits of dispersal do not differ between males and females in this species. Since levels of inbreeding in the population were low, we also determined whether the pikas chose mates based on genetic dissimilarity, and whether they decreased the inbreeding coefficients of their offspring by going on forays to mate with animals other than their neighbours. Pikas did not restrict themselves to mating with their neighbours, but the average relatedness coefficients between pairs that produced offspring did not differ from the average relatedness coefficients expected under a model of random mate choice.

Sexual antagonism for testosterone maintains multiple mating behaviour

1. The persistence of multiple mating remains one of the fundamental questions in evolutionary biology. In theory, multiple mating is predicted to improve female fitness cumulatively through direct and/or genetic benefits. However, intra-locus sexual conflicts may potentially constrain or even eliminate these benefits owing to the gender load imposed by sexually antagonistic selection. 2. Here, we tested whether sexually antagonistic selection can maintain the variance in multiple mating behaviour of bank voles (Myodes glareolus) by manipulating the hormone testosterone through artificial selection in the laboratory. Among mammals, testosterone is a sexually dimorphic fitness-related trait under selection and is known to affect mating behaviour. We conducted mating trials in which females derived from family-based selection of testosterone were sequentially paired with four males of different testosterone profiles. 3. We show that artificial selection for high testosterone increased the mating rate of males, but clearly decreased the number of partners that females mated with (and vice versa). Because multiple mating was beneficial for the reproductive success of both sexes, as evidenced by the positive Bateman gradients, the divergent evolutionary interests of testosterone between the sexes can maintain this polygynandrous mating system. 4. Our results highlight how mating rate is concordantly selected in both sexes; however, it is largely influenced by testosterone, which is under sexually antagonistic selection. 5. This study is the first one to emphasise the direct and indirect effects of the endocrine system not only on reproductive physiology and behaviour but also for the evolution of genetic mating strategies in mammals.