Good genes, genetic compatibility and the evolution of polyandry: use of the diallel cross to address competing hypotheses

Genetic benefits can enhance the fitness of polyandrous females through the high intrinsic genetic quality of females' mates or through the interaction between female and male genes. I used a full diallel cross, a quantitative genetics design that involves all possible crosses among a set of genetically homogeneous lines, to determine the mechanism through which polyandrous female decorated crickets (Gryllodes sigillatus) obtain genetic benefits. I measured several traits related to fitness and partitioned the phenotypic variance into components representing the contribution of additive genetic variance ('good genes'), nonadditive genetic variance (genetic compatibility), as well as maternal and paternal effects. The results reveal a significant variance attributable to both nonadditive and additive sources in the measured traits, and their influence depended on which trait was considered. The lack of congruence in sources of phenotypic variance among these fitness-related traits suggests that the evolution and maintenance of polyandry are unlikely to have resulted from one selective influence, but rather are the result of the collective effects of a number of factors.     

Polyandrous females provide sons with more competitive sperm: Support for the sexy‐sperm hypothesis in the rattlebox moth (Utetheisa ornatrix)

Given the costs of multiple mating, why has female polyandry evolved? Utetheisa ornatrix moths are well suited for studying multiple mating in females because females are highly polyandrous over their life span, with each male mate transferring a substantial spermatophore with both genetic and nongenetic material. The accumulation of resources might explain the prevalence of polyandry in this species, but another, not mutually exclusive, possibility is that females mate multiply to increase the probability that their sons will inherit more‐competitive sperm. This latter “sexy‐sperm” hypothesis posits that female multiple mating and male sperm competitiveness coevolve via a Fisherian runaway process. We tested the sexy‐sperm hypothesis by using competitive double matings to compare the sperm competition success of sons of polyandrous versus monandrous females. In accordance with sexy‐sperm theory, we found that in 511 offspring across 17 families, the male whose polyandrous mother mated once with each of three different males sired significantly more of all total offspring (81%) than did the male whose monandrous mother was mated thrice to a single male. Interestingly, sons of polyandrous mothers had a significantly biased sex ratio of their brood toward sons, also in support of the hypothesis.     

Additive genetic variance in polyandry enables its evolution,but polyandry is unlikely to evolve through sexy or good sperm processes

Polyandry is widespread despite its costs. The sexually selected sperm hypotheses (‘sexy’ and ‘good’ sperm) posit that sperm competition plays a role in the evolution of polyandry. Two poorly studied assumptions of these hypotheses are the presence of additive genetic variance in polyandry and sperm competitiveness. Using a quantitative genetic breeding design in a natural population of Drosophila melanogaster, we first established the potential for polyandry to respond to selection. We then investigated whether polyandry can evolve through sexually selected sperm processes. We measured lifetime polyandry and offensive sperm competitiveness (P₂) while controlling for sampling variance due to male × male × female interactions. We also measured additive genetic variance in egg‐to‐adult viability and controlled for its effect on P₂ estimates. Female lifetime polyandry showed significant and substantial additive genetic variance and evolvability. In contrast, we found little genetic variance or evolvability in P₂ or egg‐to‐adult viability. Additive genetic variance in polyandry highlights its potential to respond to selection. However, the low levels of genetic variance in sperm competitiveness suggest that the evolution of polyandry may not be driven by sexy sperm or good sperm processes.     

The more the better – polyandry and genetic similarity are positively linked to reproductive success in a natural population of terrestrial salamanders (Salamandra salamandra)

Although classically thought to be rare, female polyandry is widespread and may entail significant fitness benefits. If females store sperm over extended periods of time, the consequences of polyandry will depend on the pattern of sperm storage, and some of the potential benefits of polyandry can only be realized if sperm from different males is mixed. Our study aimed to determine patterns and consequences of polyandry in an amphibian species, the fire salamander, under fully natural conditions. Fire salamanders are ideal study objects, because mating, fertilization and larval deposition are temporally decoupled, females store sperm for several months, and larvae are deposited in the order of fertilization. Based on 18 microsatellite loci, we conducted paternity analysis of 24 female‐offspring arrays with, in total, over 600 larvae fertilized under complete natural conditions. More than one‐third of females were polyandrous and up to four males were found as sires. Our data clearly show that sperm from multiple males is mixed in the female's spermatheca. Nevertheless, paternity is biased, and the most successful male sires on average 70% of the larvae, suggesting a ‘topping off’ mechanism with first‐male precedence. Female reproductive success increased with the number of sires, most probably because multiple mating ensured high fertilization success. In contrast, offspring number was unaffected by female condition and genetic characteristics, but surprisingly, it increased with the degree of genetic relatedness between females and their sires. Sires of polyandrous females tended to be genetically similar to each other, indicating a role for active female choice.     

Genetic benefits of extreme sequential polyandry in a terrestrial‐breeding frog

Sequential polyandry may evolve as an insurance mechanism to reduce the risk of females choosing mates who are genetically inferior (intrinsic male quality hypothesis) or genetically incompatible (genetic incompatibility hypothesis). The prevalence of such indirect benefits remains controversial, however, because studies estimating the contributions of additive and nonadditive sources of genetic variation to offspring fitness have been limited to a small number of taxonomic groups. Here, we used artificial fertilization techniques combined with a crossclassified breeding design (North Carolina Type II) to simultaneously test the “good genes hypothesis” and the “genetic incompatibility hypothesis” in the brown toadlet (Pseudophryne bibronii); a terrestrial‐breeding species with extreme sequential polyandry. Our results revealed no significant additive or nonadditive genetic effects on fertilization success. Moreover, they revealed no significant additive genetic effects, but highly significant nonadditive genetic effects (sire by dam interaction effects), on hatching success and larval survival to initial and complete metamorphosis. Taken together, these results indicate that offspring viability is significantly influenced by the combination of parental genotypes, and that negative interactions between parental genetic elements manifest during embryonic and larval development. More broadly, our findings provide quantitative genetic evidence that insurance against genetic incompatibility favors the evolution and maintenance of sequential polyandry.     

DO WOLBACHIA‐ASSOCIATED INCOMPATIBILITIES PROMOTE POLYANDRY?

The genetic incompatibility avoidance hypothesis as an explanation for the polyandrous mating strategies (mating with more than one male) of females of many species has received significant attention in recent years. It has received support from both empirical studies and a meta-analysis, which concludes that polyandrous females enjoy increased reproductive success through improved offspring viability relative to monandrous females. In this study we investigate whether polyandrous female Drosophila simulans improve their fitness relative to monandrous females in the face of severe Wolbachia-associated reproductive incompatibilities. We use the results of this study to develop models that test the predictions that Wolbachia should promote polyandry, and that polyandry itself may constrain the spread of Wolbachia. Uniquely, our models allow biologically relevant rates of incompatibility to coevolve with a polyandry modifier allele, which allows us to evaluate the fate of the modifier and that of Wolbachia. Our empirical results reveal that polyandrous females significantly reduce the reproductive costs of Wolbachia, owing to infected males being poor sperm competitors. The models show that this disadvantage in sperm competition can inhibit or prevent the invasion of Wolbachia. However, despite the increased reproductive success obtained by polyandrous females, the spread of a polyandry modifier allele is constrained by any costs that might be associated with polyandry and the low frequency of incompatible matings when Wolbachia has reached a stable equilibrium. Therefore, although incompatibility avoidance may be a benefit of polyandry, our findings do not support the hypothesis that genetic incompatibilities caused by Wolbachia promote the evolution of polyandry.     

Good genes and the maternal effects of polyandry on offspring reproductive success in the bulb mite

Genetic benefits are potentially the most robust explanation of the controversial issue of evolutionary maintenance of polyandry, but the unambiguous demonstration of such benefits has been hindered by the possibility of their confusion with maternal effects. Previous research has shown that polyandrous bulb mite females produce daughters with higher fecundity than monandrous females. Here, we investigate whether this effect arises because polyandrous females invest more in their offspring, or because their offspring inherit 'good genes' from their fathers. Females were mated with either one or four (different) males. However, by sterilizing three of the four males with ionizing radiation, we eliminated any chance of sexual selection (in the polyandrous treatment) so that any differences in the female mating regimes must have been owing to maternal effects. Polyandry had no significant effect on daughter fecundity, thus indicating that any previously documented effects must have been genetic. This was further supported by a significant association between fathers' offensive sperm-competitive ability and the fecundity of their daughters. The association with fathers' sperm defensive ability was not significant, and neither was the association between fathers' sperm competitiveness and sons' reproductive success. However, sons of polyandrous females had lower reproductive success than sons of monandrous females. This shows that the maternal effects of polyandry should be taken into account whenever its costs and benefits are being considered.     

The evolution of polyandry: intrinsic sire effects contribute to embryo viability

Females typically mate with more than one male despite the costs incurred, thus questioning Bateman's principle. A series of genetic benefits have been proposed to account for the evolution of polyandry, including the acquisition of viability genes for offspring. The 'intrinsic male quality' hypothesis suggests that polyandry increases the probability that females produce offspring sired by males that bestow high viability on their offspring. Heritable variation in viability is the basic requirement for the occurrence of this genetic benefit. By using a half-sib breeding design with a species of cricket in which polyandry is known to increase hatching success, we present clear experimental evidence that intrinsic male quality contributes to embryo viability. Despite recent support for the evolution of polyandry based on compatibility of genotypes between males and females, we show that hatching success is not determined by an interaction between paternal and maternal genotypes but rather that sons inherit paternal genes that influence the viability of eggs laid by their mates. Moreover, our data implicate a potential role for indirect genetic effects of male accessory gland products on embryo viability. Additive genetic contributions to embryo viability may be an important factor underlying the frequently observed benefits of polyandrous behaviour.     

Shorter sperm confer higher competitive fertilization success

Spermatozoa exhibit taxonomically widespread patterns of divergent morphological evolution. However, the adaptive significance of variation in sperm morphology remains unclear. In this study we examine the role of natural variation in sperm length on fertilization success in the dung beetle Onthophagus taurus. We conducted sperm competition trials between males that differed in the length of their sperm and determined the paternity of resulting offspring using amplified fragment length polymorphism (AFLP) markers. We also quantified variation in the size and shape of the female's sperm storage organ to determine whether female morphology influenced the competitiveness of different sperm morphologies. We found that fertilization success was biased toward males with relatively shorter sperm, but that selection on sperm length was dependent on female tract morphology; selection was directional for reduced sperm length across most of the spermathecal size range, but stabilizing in females with the smallest spermathecae. Our data provide empirical support for the theory that sperm competition should favor the evolution of numerous tiny sperm. Moreover, because sperm length is both heritable and genetically correlated with condition, our results are consistent with a process by which females can accrue genetic benefits for their offspring from the incitement of sperm competition and/or cryptic female choice, as proposed by the "sexy sperm" and "good sperm" models for the evolution of polyandry.     

Fitness consequences of parental compatibility in the frog Crinia georgiana

Theory suggests that multiple mating by females can evolve as a mechanism for acquiring compatible genes that promote offspring fitness. Genetic compatibility models predict that differences in fitness among offspring arise from interactions between male and female haplotypes. Using a cross-classified breeding design and in vitro fertilization, we raised families of maternal and paternal half-siblings of the frog Crinia georgiana, a species with a polyandrous breeding system and external fertilization. After controlling for variation in maternal provisioning, we found significant effects of interacting parental haplotypes on fertilization success, and nonadditive genetic effects on measures of offspring fitness such as embryo survival, and survival to, size at, and time to metamorphosis. Additive genetic variation due to males and females was negligible, and not statistically significant for any of the fitness traits measured. Combinations of parental haplotypes that resulted in high rates of fertilization produced offspring with higher embryo survival and rapid juvenile development. We suggest that a gamete recognition mechanism for selective fertilization by compatible sperm may promote offspring fitness in this system.     

Context-dependent genetic benefits of polyandry in a marine hermaphrodite

Numerous studies emphasize the potential indirect (genetic) benefits of polyandry in animals with resource-free mating systems. In this paper, we examine the potential for these benefits to fuel sexual selection and polyandry in the hermaphroditic ascidian Pyura stolonifera. Individuals were designated either sire (sperm producers) or dam (egg producers) at random and crossed in a North Carolina II breeding design to produce both paternal and maternal half siblings for our quantitative genetic analysis. We then partitioned the phenotypic variance in fertilization and hatching rates into additive and non-additive variance components. We found significant additive variance attributable to sire and dam effects at fertilization and hatching, suggesting the potential for selection to favour individuals carrying intrinsically 'good genes' for these traits. In separate analyses involving monandrous and polyandrous clutches, we found that both traits were elevated under polyandry, but the difference in hatching rates was due entirely to the difference in fertilization rates between treatments. When the hatching rates were standardized to account for variance at fertilization, there was no overall net benefit of polyandry for this trait. Despite this, we found that hatching success declined with increasing embryo densities, and that the slope of this decline was significantly greater in monandrous than polyandrous clutches. Hence, selection on embryo viability may still favour polyandry under restricted environmental conditions. Nevertheless, our results caution against interpreting elevated hatching success as an indirect genetic benefit of polyandry when variance in fertilization is not controlled.     

BENEFITS OF MULTIPLE MATES IN THE CRICKET GRYLLUS BIMACULATUS

Despite the importance of polyandry for sexual selection, the reasons why females frequently mate with several males remain poorly understood. A number of genetic benefits have been proposed, based on the idea that by taking multiple mates, females increase the likelihood that their offspring will be sired by genetically more compatible or superior males. If certain males have intrinsically “good genes,” any female mating with them will produce superior offspring. Alternatively, if some males have genetic elements that are incompatible with a particular female, then she may benefit from polyandry if the sperm of such males are less likely to fertilize her eggs. We examined these hypotheses in the field cricket Gryllus bimaculatus (Orthoptera: Gryllidae). By allocating females identical numbers of matings but different numbers of mates we investigated the influence of number of mates on female fecundity, and both short- and long-term offspring fitness. This revealed no effect of number of mates on number of eggs laid. However, hatching success of eggs increased with number of mates. This effect could not be attributed to nongenetic effects such as the possibility that polyandry reduces variance in the quantity or fertilizing ability of sperm females receive, because a control group receiving half the number of copulations showed no drop in hatching success. Offspring did not differ in survival, adult mass, size, or development time with treatment. When males were mated to several different females there were no repeatable differences between individual males in the hatching success of their mate's eggs. This suggests that improved hatching success of polyandrous females is not due to certain males having genes that improve egg viability regardless of their mate. Instead, our results support the hypothesis that certain males are genetically more compatible with certain females, and that this drives polyandry through differential fertilization success of sperm from more compatible males.     

Polyandry and fitness of offspring reared under varying nutritional stress in decorated crickets

Abstract.— Females, by mating with more than one male in their lifetime, may reduce their risk of receiving sperm from genetically incompatible sires or increase their prospects of obtaining sperm from genetically superior sires. Although there is evidence of both kinds of genetic benefits in crickets, their relative importance remains unclear, and the extent to which experimentally manipulated levels of polyandry in the laboratory correspond to those that occur in nature remain unknown. We measured lifetime polyandry of free-living female decorated crickets, Gryllodes sigillatus , and conducted an experiment to determine whether polyandry leads to an increase in offspring viability. We experimentally manipulated both the levels of polyandry and opportunities for females to select among males, randomly allocating the offspring of experimental females to high-food-stress or low-food-stress regimes to complete their development. Females exhibited a high degree of polyandry, mating on average with more than seven different males during their lifetime and up to as many as 15. Polyandry had no effect on either the developmental time or survival of offspring. However, polyandrous females produced significantly heavier sons than those of monandrous females, although there was no difference in the adult mass of daughters. There was no significant interaction between mating treatment and offspring nutritional regimen in their effects on offspring mass, suggesting that benefits accruing to female polyandry are independent of the environment in which offspring develop. The sex difference in the extent to which male and female offspring benefit via their mother's polyandry may reflect possible differences in the fitness returns from sons and daughters. The larger mass gain shown by sons of polyandrous females probably leads to their increased reproductive success, either because of their increased success in sperm competition or because of their increased life span.     

Male house mice evolving with post-copulatory sexual selection sire embryos with increased viability

Although mating is costly, multiple mating by females is a taxonomically widespread phenomenon. Theory has suggested that polyandry may allow females to gain genetic benefits for their offspring, and thus offset the costs associated with this mating strategy. For example, the good sperm hypothesis posits that females benefit from mating multiply when genetically superior males have increased success in sperm competition and produce high quality offspring. We applied the powerful approach of experimental evolution to explore the potential for polyandry to drive evolutionary increases in female fitness in house mice, Mus domesticus. We maintained polygamously mated and monogamously mated selection lines of house mice for 14 generations, before determining whether selection history could account for divergence in embryo viability. We found that males from lineages evolving with post-copulatory sexual selection sire offspring with increased viability, suggesting that polyandry results in the production of higher quality offspring and thus provides long-term fitness benefits to females.     

PATTERNS OF PATERNITY SKEW AMONG POLYANDROUS SOCIAL INSECTS: WHAT CAN THEY TELL US ABOUT THE POTENTIAL FOR SEXUAL SELECTION?

Monogamy results in high genetic relatedness among offspring and thus it is generally assumed to be favored by kin selection. Female multiple mating (polyandry) has nevertheless evolved several times in the social Hymenoptera (ants, bees, and wasps), and a substantial amount of work has been conducted to understand its costs and benefits. Relatedness and inclusive fitness benefits are, however, not only influenced by queen mating frequency but also by paternity skew, which is a quantitative measure of paternity biases among the offspring of polyandrous females. We performed a large‐scale phylogenetic analysis of paternity skew across polyandrous social Hymenoptera. We found a general and significant negative association between paternity frequency and paternity skew. High paternity skew, which increases relatedness among colony members and thus maximizes inclusive fitness gains, characterized species with low paternity frequency. However, species with highly polyandrous queens had low paternity skew, with paternity equalized among potential sires. Equal paternity shares among fathers are expected to maximize fitness benefits derived from genetic diversity among offspring. We discuss the potential for postcopulatory sexual selection to influence patterns of paternity in social insects, and suggest that sexual selection may have played a key, yet overlooked role in social evolution.     

Social polyandry, parental investment, sexual selection, and evolution of reduced female gamete size

Abstract Sexual selection in the form of sperm competition is a major explanation for small size of male gametes. Can sexual selection in polyandrous species with reversed sex roles also lead to reduced female gamete size? Comparative studies show that egg size in birds tends to decrease as a lineage evolves social polyandry. Here, a quantitative genetic model predicts that female scrambles over mates lead to evolution of reduced female gamete size. Increased female mating success drives the evolution of smaller eggs, which take less time to produce, until balanced by lowered offspring survival. Mean egg size is usually reduced and polyandry increased by increasing sex ratio (male bias) and maximum possible number of mates. Polyandry also increases with the asynchrony (variance) in female breeding start. Opportunity for sexual selection increases with the maximum number of mates but decreases with increasing sex ratio. It is well known that parental investment can affect sexual selection. The model suggests that the influence is mutual: owing to a coevolutionary feedback loop, sexual selection in females also shapes initial parental investment by reducing egg size. Feedback between sexual selection and parental investment may be common.     

The effect of female polyandry and sperm precedence on the evolution of sexual difference in dispersal timing

Predispersal copulation and unpredictable environment facilitate the evolution of female-biased dispersal in species, where females are functionally monandrous. Females should migrate and reproduce over different habitats to spread their risks due to environmental fluctuation. On the other hand, males do not have to disperse because their risks are spread by their mating partners who produce their offspring in different habitats. However, when females are functionally polyandrous, it is expected that they will not contribute to spreading the male's risk extensively. Therefore, by simulation with the individual based model, the present study evaluated how female polyandry influences the sexual difference in dispersal timing. This model revealed that when females are polyandrous, the timing of female remating and sperm priority patterns have an important influence on the evolution of sex-biased dispersal. Particularly when female remating is not synchronized with dispersal or when last-male sperm precedence does not exist, female-biased dispersal is evolved.     

Do female black field crickets Teleogryllus commodus benefit from polyandry?

Female insects that mate multiply tend to have increased lifetime fitness, apparently because of greater access to male-derived resources (e.g. sperm, nuptial gifts) that elevate fertility/fecundity. Experiments that standardize the number of matings per female also show that polyandry can improve aspects of offspring performance, most notably early embryo survival (egg hatching success). This improvement is widely attributed to genetic benefits which would arise if polyandrous females skew paternity to produce fitter offspring. In two separate experiments with field crickets (Teleogryllus commodus) polyandrous females (two, three or four mates) did not have higher egg hatching success than monandrous females (effect sizes: r = 0.03 and 0.08 for the respective experiments), which is consistent with our finding of no sire effect on hatching success. Polyandry also had no effect on post-hatching offspring survival. Polyandrous females' offspring took significantly longer to mature but their sons were not heavier and their daughters were actually significantly smaller than those of monandrous females. Finally, after controlling for relative male size, monandrous females' sons were more successful when directly competing for a mate.     

Female mate choice predicts paternity success in the absence of additive genetic variance for other female paternity bias mechanisms in Drosophila serrata

After choosing a first mate, polyandrous females have access to a range of opportunities to bias paternity, such as repeating matings with the preferred male, facilitating fertilization from the best sperm or differentially investing in offspring according to their sire. Female ability to bias paternity after a first mating has been demonstrated in a few species, but unambiguous evidence remains limited by the access to complex behaviours, sperm storage organs and fertilization processes within females. Even when found at the phenotypic level, the potential evolution of any mechanism allowing females to bias paternity other than mate choice remains little explored. Using a large population of pedigreed females, we developed a simple test to determine whether there is additive genetic variation in female ability to bias paternity after a first, chosen, mating. We applied this method in the highly polyandrous Drosophila serrata, giving females the opportunity to successively mate with two males ad libitum. We found that despite high levels of polyandry (females mated more than once per day), the first mate choice was a significant predictor of male total reproductive success. Importantly, there was no detectable genetic variance in female ability to bias paternity beyond mate choice. Therefore, whether or not females can bias paternity before or after copulation, their role on the evolution of sexual male traits is likely to be limited to their first mate choice in D. serrata.     

Implications of multiple mating for offspring relatedness and shoaling behaviour in juvenile guppies

Polyandry (female multiple mating) can confer important benefits to females, but few studies have considered its potential costs. One such cost may arise through differences in the relatedness of offspring born to females with different mating histories; offspring born to monandrous females are always full siblings, while those produced by polyandrous females may be full or half siblings. These differences may have important consequences for social interactions among offspring. We used artificial insemination in the guppy (Poecilia reticulata), a promiscuous live-bearing fish, to evaluate shoaling behaviour in polyandrous and monandrous broods. We combined this information with known parentage data for the polyandrous broods to determine whether sibling relatedness influenced offspring shoaling behaviour. While we detected no effect of mating treatment (polyandry/monandry) on shoaling behaviour, we found that pairs of full siblings spent significantly more time shoaling (and in close proximity) than pairs of half siblings. This latter finding confirms the ability of newborn guppies to distinguish brood mates on the basis of kinship, but also suggests an important and hitherto unrealized potential cost of polyandry: a reduction in within-brood relatedness with potentially important implications for offspring social behaviour.