Size breeds success: multiple paternity, multivariate selection and male semelparity in a small marsupial, Antechinus stuartii

Mating in the marsupial genus Antechinus is a synchronous annual event that is characterized by monoestry in females and abrupt postmating mortality in males. Male semelparity (multiple copulations during a single breeding season per lifetime) is often assumed to occur as a consequence of the intense mating effort expended by males in the rut, but the forces selecting for this remain elusive. Here, we investigate selection in male brown antechinus, Antechinus stuartii, and test two hypotheses for the evolution of semelparity: intermale competition and sperm competition. If intermale competition drives semelparity, we predicted that males would be under strong selection for large body size. If sperm competition is important, we predicted that selection would be strongest on scrotal size, a surrogate for testes volume. Using microsatellite markers, we found that 92% of females in free-living conditions mated with multiple males, producing litters of eight that had up to four fathers. These observations confirm the potential for sperm competition. Using selection analysis, we then found paternity success in 119 males to be related most strongly to body mass and scrotal size, thus providing support for both hypotheses. Large males presumably experience increased paternity success by gaining more matings or prolonged copulations via mate guarding, while large testes may allow increased sperm investment per copulation. Increased levels of free corticosteroid hormones in males facilitate the extreme mating effort during the short period of rut, but lead to immune suppression and consequently to the phenomenon of postmating mortality.     

Factors influencing paternity success in Antechinus agilis: last‐male sperm precedence,timing of mating and genetic compatibility

We describe the patterns of paternity success from laboratory mating experiments conducted in Antechinus agilis, a small size dimorphic carnivorous marsupial (males are larger than females). A previous study found last‐male sperm precedence in this species, but they were unable to sample complete litters, and did not take male size and relatedness into account. We tested whether last‐male sperm precedence regardless of male size still holds for complete litters. We explored the relationship between male mating order, male size, timing of mating and relatedness on paternity success. Females were mated with two males of different size with either the large or the small male first, with 1 day rest between the matings. Matings continued for 6 h. In these controlled conditions male size did not have a strong effect on paternity success, but mating order did. Males mating second sired 69.5% of the offspring. Within first mated males, males that mated closer to ovulation sired more offspring. To a lesser degree, variation appeared also to be caused by differences in genetic compatibility of the female and the male, where high levels of allele‐sharing resulted in lower paternity success.     

Adult sex ratio,sexual dimorphism and sexual selection in a Mesozoic reptile

The evolutionary history of sexual selection in the geologic past is poorly documented based on quantification, largely because of difficulty in sexing fossil specimens. Even such essential ecological parameters as adult sex ratio (ASR) and sexual size dimorphism (SSD) are rarely quantified, despite their implications for sexual selection. To enable their estimation, we propose a method for unbiased sex identification based on sexual shape dimorphism, using size-independent principal components of phenotypic data. We applied the method to test sexual selection in Keichousaurus hui, a Middle Triassic (about 237 Ma) sauropterygian with an unusually large sample size for a fossil reptile. Keichousaurus hui exhibited SSD biased towards males, as in the majority of extant reptiles, to a minor degree (sexual dimorphism index −0.087). The ASR is about 60% females, suggesting higher mortality of males over females. Both values support sexual selection of males in this species. The method may be applied to other fossil species. We also used the Gompertz allometric equation to study the sexual shape dimorphism of K. hui and found that two sexes had largely homogeneous phenotypes at birth except in the humeral width, contrary to previous suggestions derived from the standard allometric equation.     

Long-term paternity skew and the opportunity for selection in a mammal with reversed sexual size dimorphism

Most mammalian groups are characterized by male-biased sexual size dimorphism, in which size-dependent male-male competition and reproductive skew are tightly linked. By comparison, little is known about the opportunity for sexual selection in mammalian systems without male-biased dimorphism, where the traits under sexual selection might be less obvious. We examined 10 years of parentage data in a colony of greater horseshoe bats (Rhinolophus ferrumequinum) to determine the magnitude of male reproductive skew and the opportunity for sexual selection in a mammal in which females are the larger sex. Annual paternity success was weakly skewed but consistent patterns led to strong longitudinal paternity skew among breeders. Just three males accounted for a third of all paternity assignments, representing at least a fifth of all colony offspring born in a decade. Paternity success was in part determined by age but was not influenced by dispersal status. Our results show that paternity skew and the opportunity for sexual selection in a species with reversed sexual size dimorphism can approach levels reported for classical examples of species with polygyny and male-biased dimorphism, even where the traits under sexual selection are not known.     

Operational sex ratio, sexual conflict and the intensity of sexual selection

Modern sexual selection theory indicates that reproductive costs rather than the operational sex ratio predict the intensity of sexual selection. We investigated sexual selection in the polygynandrous common lizard Lacerta vivipara . This species shows male aggression, causing high mating costs for females when adult sex ratios (ASR) are male-biased. We manipulated ASR in 12 experimental populations and quantified the intensity of sexual selection based on the relationship between reproductive success and body size. In sharp contrast to classical sexual selection theory predictions, positive directional sexual selection on male size was stronger and positive directional selection on female size weaker in female-biased populations than in male-biased populations. Thus, consistent with modern theory, directional sexual selection on male size was weaker in populations with higher female mating costs. This suggests that the costs of breeding, but not the operational sex ratio, correctly predicted the strength of sexual selection.     

More than just noise: Chance,mating success,and sexual selection

Chance plays a critical but underappreciated role in determining mating success. In many cases, we tend to think of chance as background noise that can be ignored in studies of mating dynamics. When the influence of chance is consistent across contexts, chance can be thought of as background noise; in other cases, however, the impact of chance on mating success can influence our understanding of how mates are acquired and how sexual selection operates. In particular, when the importance of chance covaries with biological or ecological factors in a systematic manner—that is, when chance becomes consistently more or less important under certain conditions—then chance is important to consider if we want to fully understand the operation of mate acquisition and sexual selection. Here, we present a model that explores how chance covaries with factors such as sex ratio, adult population size, and mating regime in determining variation in mating success. We find that in some cases, chance covaries with adult population size and the operational sex ratio to create variation in mating success. We discuss how chance can influence our more general understanding of the operation of mating dynamics and sexual selection.     

The effects of habitat fragmentation via forestry plantation establishment on spatial genotypic structure in the small marsupial carnivore, Antechinus agilis

Dispersal is an important influence on species' distributions, patch colonization and population persistence in fragmented habitat. We studied the impacts of habitat fragmentation resulting from establishment of an exotic pine plantation on dispersal of the marsupial carnivore, Antechinus agilis. We applied spatial analyses of individual multilocus microsatellite genotypes and mitochondrial haplotypes to study patterns of gene flow in fragmented habitat and natural habitat 'control' areas, and how this is affected by the spatial dispersion of habitat patches, the presence of corridors and a 'mainland' source of migrants. Spatial analysis of molecular variance and partial Mantel tests confirmed the absence of cryptic barriers to gene flow in continuous habitat, which if present would confound the comparison of genetic structures in fragmented vs. unfragmented habitats. Spatial genotypic structure suggested that although dispersal was male-biased in both habitat types, fragmentation restricted dispersal of males more than that of females and the degree of restriction of male dispersal was dependent on the geographical isolation of the patch. The scale of positive genotypic structure in fragmented habitat was restricted to the two closest patches for females and the three closest patches for males. Our results provide evidence for significantly increased gene flow through habitat corridors relative to that across the matrix and for significantly lower gene flow between 'mainland' unfragmented habitat and habitat patches relative to that within either habitat type, suggesting a behavioural barrier to crossing habitat interfaces.     

The effects of habitat fragmentation on the social kin structure and mating system of the agile antechinus, Antechinus agilis

Habitat fragmentation is one of the major contributors to the loss of biodiversity worldwide. However, relatively little is known about its more immediate impacts on within-patch population processes such as social structure and mating systems, whose alteration may play an important role in extinction risk. We investigated the impacts of habitat fragmentation due to the establishment of an exotic softwood plantation on the social kin structure and breeding system of the Australian marsupial carnivore, Antechinus agilis. Restricted dispersal by males in fragmented habitat resulted in elevated relatedness among potential mates in populations in fragments, potentially increasing the risk of inbreeding. Antechinus agilis nests communally in tree hollows; these nests are important points for social contact between males and females in the mating season. In response to elevated relatedness among potential mates in fragmented habitat, A. agilis significantly avoided sharing nests with opposite-sex relatives in large fragment sites (but not in small ones, possibly due to limited nest locations and small population sizes). Because opposite-sex individuals shared nests randomly with respect to relatedness in unfragmented habitat, we interpreted the phenomenon in fragmented habitat as a precursor to inbreeding avoidance via mate choice. Despite evidence that female A. agilis at high inbreeding risk selected relatively unrelated mates, there was no overall increased avoidance of related mates by females in fragmented habitats compared to unfragmented habitats. Simulations indicated that only dispersal, and not nonrandom mating, contributed to inbreeding avoidance in either habitat context. However, habitat fragmentation did influence the mating system in that the degree of multiple paternity was reduced due to the reduction in population sizes and population connectivity. This, in turn, reduced the number of males available to females in the breeding season. This suggests that in addition to the obvious impacts of reduced recruitment, patch recolonization and increased genetic drift, the isolation of populations in habitat patches may cause changes in breeding behaviour that contribute to the negative impacts of habitat fragmentation.     

Male Red-winged Blackbirds with experimentally dulled epaulets experience no disadvantage in sexual selection

ABSTRACT.   The epaulets of male Red-winged Blackbirds ( Agelaius phoeniceus ) are frequently cited as a sexually selected plumage ornament, but a number of laboratory and field studies provide little evidence that they are currently experiencing sexual selection. We used hair dye to dull epaulets of free-living territorial males prior to pair formation to determine if manipulated males experienced disadvantages in comparison with control males. We found no differences between control males and males with dulled epaulets in territorial behavior (territory size, song rate, trespass rate, and loss of territory), paternal care (time spent on territory and in antipredator sentinel behavior, and response to a model crow to simulate the threat of predation), pairing success (number of social mates), apparent reproductive success (numbers of nesting attempts, eggs/nest, nestlings/egg, and fledglings/nestling), or realized reproductive success (numbers of within-pair, extra-pair, and total fledglings as determined by DNA fingerprinting). We then used a meta-analysis of 11 published studies of Red-winged Blackbirds to determine if there is an overall effect of epaulet color or size on male-male competition, female choice, or reproductive success. Our results show that epaulet size has a small positive effect on male reproductive success, but epaulet color has no effect on male-male competition, female choice, and male reproductive success. One explanation for the seeming contradiction between studies that show that epaulets are necessary for territory defense and those that conclude that epaulets are not currently under selection is that epaulets serve as one of several cues of species recognition, especially among males at close range. An alternative explanation proposes counter-balancing intersexual advantages and intrasexual disadvantages of epaulet expression. Additional studies are needed to test these alternatives.     

Operational sex ratio influences the opportunity for sexual selection in guppies

The opportunity for sexual selection was greater when the operational sex ratio (OSR) in guppies Poecilia reticulata was biased towards males. This could be due to an increase in both male-male competition and female mate choice under male-biased OSR.     

Sexual size dimorphism and sexual selection in primates

1. In most animals, females are larger than males. Paradoxically, sexual size dimorphism is biased towards males in most mammalian species. An accepted explanation is that sexual dimorphism in mammals evolved by intramale sexual selection. I tested this hypothesis in primates, by relating sexual size dimorphism to seven proxies of sexual selection intensity: operational sex ratio, mating system, intermale competition, group sex ratio, group size, maximum mating percentage (percentage of observed copulations involving the most successful male), and total paternity (a genetic estimate of the percentage of young sired by the most successful male).
2. I fitted phylogenetic generalised least squares models using sexual size dimorphism as the dependent variable and each of the seven measures of intensity of sexual selection as independent variables. I conducted this comparative analysis with data from 50 extant species of primates, including Homo sapiens, Pan troglodytes, and Gorilla spp.
3. Sexual dimorphism was positively related to the four measures of female monopolisation (operational sex ratio, mating system, intermale competition, and group sex ratio) and in some cases to group size, but was not associated with maximum mating percentage or total paternity. Additional regression analyses indicated that maximum mating percentage and total paternity were negatively associated with group size.
4. These results are predicted by reproductive skew theory: in large groups, males can lose control of the sexual behaviour of the other members of the group or can concede reproductive opportunities to others. The results are also consistent with the evolution of sexual size dimorphism before polygyny, due to the effects of natural, rather than sexual, selection. In birds, the study of molecular paternity showed that variance in male reproductive success is much higher than expected by behaviour. In mammals, recent studies have begun to show the opposite trend, i.e. that intensity of sexual selection is lower than expected by polygyny.
5. Results of this comparative analysis of sexual size dimorphism and sexual selection intensity in primates suggest that the use of intramale sexual selection theory to explain the evolution of polygyny and sexual dimorphism in mammals should be reviewed, and that natural selection should be considered alongside sexual selection as an evolutionary driver of sexual size dimorphism and polygyny in mammals.

     

Male mating success, reproductive success and multiple paternity in a natural population of sand lizards: behavioural and molecular genetics data

Sand lizard Lacerta agilis females characteristically mate with several males which, in staged mating experiments, results in multiple paternity of the offspring. In order to investigate multiple paternity in a natural population and interpret male reproductive behaviours in terms of sired young, we sampled the blood of females, potential fathers and hatchlings, and determined paternity using multilocus DNA fingerprinting as well as the variation at a single locus detected by the probe (TC) _n . The paternity analyses were preceded by a laboratory experiment in which we established that the parental alleles identified by the single locus probe were inherited in a Mendelian way. Our molecular data demonstrated that 12 out of 13 males (92%) that sired offspring were correctly identified from the 56 sexually mature males in the population. Also smaller males were accepted as sexual partners by the females, but sired fewer young in competition with larger males and were less able to maintain prolonged post-copulatory mate guarding. This may result in that some sexually successful males are only observed inside a female's home range, but never in pair-association with the female.     

The mismeasurement of sexual selection

Sexual selection can explain major micro‐ and macro‐evolutionary patterns. Much of current theory predicts that the strength of sexual selection (i) is driven by the relative abundance of males and females prepared to mate (i.e. the operational sex ratio, OSR) and (ii) can be generally estimated by calculating intra‐sexual variation in mating success (e.g. the opportunity for sexual selection, I_s). Here, we demonstrate the problematic nature of these predictions. The OSR and I_s only accurately predict sexual selection under a limited set of circumstances, and more specifically, only when mate monopolization is extremely strong. If mate monopolization is not strong, using OSR or I_s as proxies or measures of sexual selection is expected to produce spurious results that lead to the false conclusion that sexual selection is strong when it is actually weak. These findings call into question the validity of empirical conclusions based on these measures of sexual selection.     

Reproductive skew drives patterns of sexual dimorphism in sponge-dwelling snapping shrimps

Sexual dimorphism is typically a result of strong sexual selection on male traits used in male–male competition and subsequent female choice. However, in social species where reproduction is monopolized by one or a few individuals in a group, selection on secondary sexual characteristics may be strong in both sexes. Indeed, sexual dimorphism is reduced in many cooperatively breeding vertebrates and eusocial insects with totipotent workers, presumably because of increased selection on female traits. Here, we examined the relationship between sexual dimorphism and sociality in eight species of Synalpheus snapping shrimps that vary in social structure and degree of reproductive skew. In species where reproduction was shared more equitably, most members of both sexes were physiologically capable of breeding. However, in species where reproduction was monopolized by a single individual, a large proportion of females—but not males—were reproductively inactive, suggesting stronger reproductive suppression and conflict among females. Moreover, as skew increased across species, proportional size of the major chela—the primary antagonistic weapon in snapping shrimps—increased among females and sexual dimorphism in major chela size declined. Thus, as reproductive skew increases among Synalpheus, female–female competition over reproduction appears to increase, resulting in decreased sexual dimorphism in weapon size.     

Parental investment, sexual selection and sex ratios

Conventional sex roles imply caring females and competitive males. The evolution of sex role divergence is widely attributed to anisogamy initiating a self‐reinforcing process. The initial asymmetry in pre‐mating parental investment (eggs vs. sperm) is assumed to promote even greater divergence in post‐mating parental investment (parental care). But do we really understand the process? Trivers [Sexual Selection and the Descent of Man 1871–1971 (1972), Aldine Press, Chicago] introduced two arguments with a female and male perspective on whether to care for offspring that try to link pre‐mating and post‐mating investment. Here we review their merits and subsequent theoretical developments. The first argument is that females are more committed than males to providing care because they stand to lose a greater initial investment. This, however, commits the ‘Concorde Fallacy’ as optimal decisions should depend on future pay‐offs not past costs. Although the argument can be rephrased in terms of residual reproductive value when past investment affects future pay‐offs, it remains weak. The factors likely to change future pay‐offs seem to work against females providing more care than males. The second argument takes the reasonable premise that anisogamy produces a male‐biased operational sex ratio (OSR) leading to males competing for mates. Male care is then predicted to be less likely to evolve as it consumes resources that could otherwise be used to increase competitiveness. However, given each offspring has precisely two genetic parents (the Fisher condition), a biased OSR generates frequency‐dependent selection, analogous to Fisherian sex ratio selection, that favours increased parental investment by whichever sex faces more intense competition. Sex role divergence is therefore still an evolutionary conundrum. Here we review some possible solutions. Factors that promote conventional sex roles are sexual selection on males (but non‐random variance in male mating success must be high to override the Fisher condition), loss of paternity because of female multiple mating or group spawning and patterns of mortality that generate female‐biased adult sex ratios (ASR). We present an integrative model that shows how these factors interact to generate sex roles. We emphasize the need to distinguish between the ASR and the operational sex ratio (OSR). If mortality is higher when caring than competing this diminishes the likelihood of sex role divergence because this strongly limits the mating success of the earlier deserting sex. We illustrate this in a model where a change in relative mortality rates while caring and competing generates a shift from a mammalian type breeding system (female‐only care, male‐biased OSR and female‐biased ASR) to an avian type system (biparental care and a male‐biased OSR and ASR).     

Gamete traits influence the variance in reproductive success, the intensity of sexual selection, and the outcome of sexual conflict among congeneric sea urchins

Sea-urchin species differ in susceptibility to sperm limitation and polyspermy, but the influences of gamete traits on reproductive variance, sexual selection, and sexual conflict are unknown. I compared male and female reproductive success of two congeners at natural densities in the sea. The eggs of the species occurring at higher densities, Strongylocentrotus purpuratus, require higher sperm concentrations for fertilization but are more resistant to polyspermy compared to S. franciscanus. Both species show high variance in male fertilization success at all densities and high variance in female success at low densities, but they differ in female variance at high densities, where only S. franciscanus shows high female variance. The intensity of sexual selection based on Bateman gradients is high in males of both species, variable in S. franciscanus females, and low in S. purpuratus females. Strongylocentrotus franciscanus females experience sexual selection at low densities and sexual conflict at high densities. Strongylocentrotus purpuratus may rarely experience sperm limitation and may have evolved to ameliorate sexual conflict. This reduces the variance in female fertilization, providing females with more control over fertilization. Sperm availability influences sexual selection directly by determining sperm-egg encounter probabilities and indirectly through selection on gamete traits that alter reproductive variances.     

Operational sex ratio and density do not affect directional selection on male sexual ornaments and behavior

Demographic parameters including operational sex ratio (OSR) and population density may influence the opportunity for, and strength of sexual selection. Traditionally, male-biased OSRs and high population densities have been thought to increase the opportunity for sexual selection on male sexual traits due to increased male competition for mates. Recent experimental evidence, however, suggests that male-biased OSRs might reduce the opportunity for sexual selection due to increased sexual coercion experienced by females. How OSR, density, and any resultant changes in the opportunity for sexual selection actually affect selection on male sexual traits is unclear. In this study, we independently manipulated OSR and density in the guppy (Poecilia reticulata) without altering the number of males present. We recorded male and female behavior and used DNA microsatellite data to assign paternity to offspring and estimate male reproductive success. We then used linear selection analyses to examine the effects of OSR and density on directional sexual selection on male behavioral and morphological traits. We found that females were pursued more by males in male-biased treatments, despite no change in individual male behavior. There were no differences in sexual behavior experienced by females or performed by males in relation to density. Neither OSR nor density significantly altered the opportunity for sexual selection. Also, Although there was significant multivariate linear selection operating on males, neither OSR nor density altered the pattern of sexual selection on male traits. Our results suggest that differences in either OSR or density (independent of the number of males present) are unlikely to alter directional evolutionary change in male sexual traits.     

Female-biased sexual size dimorphism in the yellow-pine chipmunk (Tamias amoenus): sex-specific patterns of annual reproductive success and survival

Sexual size dimorphism is ultimately the result of independent, sex-specific selection on body size. In mammals, male-biased sexual size dimorphism is the predominant pattern, and it is usually attributed to the polygynous mating system prevalent in most mammals. This sole explanation is unsatisfying because selection acts on both sexes simultaneously, therefore any explanation of sexual size dimorphism should explain why one sex is relatively large and the other is small. Using mark-recapture techniques and DNA microsatellite loci to assign parentage, we examined sex-specific patterns of annual reproductive success and survival in the yellow-pine chipmunk (Tamias amoenus), a small mammal with female-biased sexual size dimorphism, to test the hypothesis that the dimorphism was related to sex differences in the relationship between body size and fitness. Chipmunks were monitored and body size components measured over three years in the Kananaskis Valley, Alberta, Canada. Male reproductive success was independent of body size perhaps due to trade-offs in body size associated with behavioral components of male mating success: dominance and running speed. Male survival was consistent with stabilizing selection for overall body size and body size components. The relationship between reproductive success and female body size fluctuated. In two of three years the relationship was positive, whereas in one year the relationship was negative. This may have been the result of differences in environmental conditions among years. Large females require more energy to maintain their soma than small females and may be unable to maintain lactation in the face of challenging environmental conditions. Female survival was positively related to body size, with little evidence for stabilizing selection. Sex differences in the relationship between body size and fitness (reproductive success and survival) were the result of different processes, but were ultimately consistent with female-biased sexual size dimorphism evident in this species.     

Competing dwarf males: sexual selection in an orb-weaving spider

Hypotheses for the adaptive significance of extreme female-biased sexual size dimorphism (SSD) generally assume that in dimorphic species males rarely interfere with each other. Here we provide the first multivariate examination of sexual selection because of male-male competition over access to females in a species with 'dwarf' males, the orb-weaving spider Argiope aurantia. Male A. aurantia typically try to mate opportunistically during the female's final moult when she is defenceless. We show that, contrary to previous hypotheses, the local operational sex ratio (males per female on the web) is male-biased most of the season. Both interference and scramble competition occur during opportunistic mating, the former leading to significant selection for large male body size. Male condition and leg length had no effect on mating success independent of size. We discuss these findings in the context of the evolution of extreme female-biased SSD in this clade.