Differential allocation in a lekking bird: females lay larger eggs and are more likely to have male chicks when they mate with less related males

The differential allocation hypothesis predicts increased investment in offspring when females mate with high-quality males. Few studies have tested whether investment varies with mate relatedness, despite evidence that non-additive gene action influences mate and offspring genetic quality. We tested whether female lekking lance-tailed manakins (Chiroxiphia lanceolata) adjust offspring sex and egg volume in response to mate attractiveness (annual reproductive success, ARS), heterozygosity and relatedness. Across 968 offspring, the probability of being male decreased with increasing parental relatedness but not father ARS or heterozygosity. This correlation tended to diminish with increasing lay-date. Across 162 offspring, egg volume correlated negatively with parental relatedness and varied with lay-date, but was unrelated to father ARS or heterozygosity. Offspring sex and egg size were unrelated to maternal age. Comparisons of maternal half-siblings in broods with no mortality produced similar results, indicating differential allocation rather than covariation between female quality and relatedness or sex-specific inbreeding depression in survival. As males suffer greater inbreeding depression, overproducing females after mating with related males may reduce fitness costs of inbreeding in a system with no inbreeding avoidance, while biasing the sex of outbred offspring towards males may maximize fitness via increased mating success of outbred sons.     

How female reed buntings benefit from extra-pair mating behaviour: testing hypotheses through patterns of paternity in sequential broods

Extra-pair paternity is an important aspect of reproductive strategies in many species of birds. Given that in most species females control whether fertilization occurs, they are expected to benefit in some way from the extra-pair matings. In this study we use patterns of extra-pair paternity (EPP) in broods of individual reed buntings (Emberiza schoeniclus), both within and between seasons, to test four hypothesized female benefits: (1) assessing potential future partners and seeking (2) genetic diversity (3) good genes, or (4) compatible genes. Reed buntings are socially monogamous, multibrooded passerines with extremely high levels of extra-pair paternity. We studied a population of reed buntings in the Netherlands in 2002 and 2003; 51% of offspring in 74% of nests were extra-pair. We showed that patterns of EPP did not support the first and second hypotheses, since females did not form a pair with previous extra-pair partners, EPP was not evenly distributed among broods and more broods than expected were sired by a single male. Furthermore, there was no relation between a male's within- and extra-pair fertilization success, no consistency in EPP between breeding attempts, no effect of parental relatedness on EPP and several cases of reciprocal paternity. These patterns do not support the good genes hypothesis and are most consistent with the genetic compatibility hypothesis. However, our previous finding that older males are more successful in gaining EPP, suggests some effect of good genes. These hypotheses need not be mutually exclusive, as females may select compatible males above a certain quality threshold (e.g. old males).     

Crickets detect the genetic similarity of mating partners via cuticular hydrocarbons

Animals should decipher information about the genetic make‐up of conspecifics in order to enhance the fitness benefits associated with mate choice. Although there is increasing evidence to suggest that animals make genetically informed decisions about their mating partners, we understand relatively little about the sensory mechanisms informing these decisions. Here, we investigate whether cuticular hydrocarbons, chemical compounds found on the cuticle of most terrestrial arthropods, provide a means of discerning genetic similarity during mate choice in the cricket, Teleogryllus oceanicus. We found that individuals preferentially mated with partners who share more dissimilar cuticular hydrocarbon profiles and that similarity in cuticular hydrocarbon profiles between mating pairs correlated with their genetic similarity. Our results provide good evidence that cuticular hydrocarbon profiles offer a means of assessing genetic compatibility in T. oceanicus, enabling individuals to choose their most genetically suitable mate.     

Complexity and context of MHC-correlated mating preferences in wild populations

There is now substantial and growing evidence for a role of the major histocompatibility complex (MHC) in shaping individual mate preferences. In view of both its codominant expression and its function in immune response, it is often expected that females aim to avoid inbreeding or maximize offspring MHC-heterozygosity by selecting as mates those males which share fewest or no MHC alleles with themselves. However, it is becoming increasingly clear that this view is over-simplistic: not only is MHC dissimilarity just one of several (perhaps many) criteria important in mate choice decision-making, extremely MHC-dissimilar males may be avoided, and furthermore, specific alleles or combinations might be preferred if they bestow particular advantages. These points are raised in two papers in this Molecular Ecology issue, in which patterns of reproductive success in tiger salamanders ( Ambystoma tigrinum ) and three-spined sticklebacks ( Gasterosteus aculeatus ) are each inconsistent with a generalized preference for MHC dissimilarity. Together, these studies demonstrate several adaptive reasons for decision rules that do not necessarily result in maximizing mate dissimilarity.     

DOES GENETIC RELATEDNESS OF MATES INFLUENCE COMPETITIVE FERTILIZATION SUCCESS IN GUPPIES?

A growing number of studies highlight the nontransitive properties of ejaculates when they are in competition to fertilize a female's eggs. Increasingly, these studies suggest that postcopulatory processes act as a filter against sperm from closely related males or those with similar genotypes, limiting the deleterious effects of inbreeding on offspring fitness. We investigated the potential for such postcopulatory mechanisms of inbreeding avoidance in the guppy (Poecilia reticulata), a promiscuous livebearing fish. We used artificial insemination as a method of delivering to a female the combined ejaculates from a first cousin (relatedness coefficient r = 0.125) and an unrelated male. This method of sperm delivery controls behavioral processes of pre- and postcopulatory female choice, which can bias paternity toward unrelated males. Our genetic analysis revealed no effect of parental relatedness on paternity outcomes. The observed mean paternity share for related males (0.47) and associated variance did not differ significantly from an expected binomial distribution that assumes no biased use of sperm with respect to relatedness (0.5). Although our data provide no evidence for postcopulatory mechanisms of inbreeding avoidance, the ability of female guppies to influence ejaculate transfer and retention offers an alternative and easily testable mechanism of inbreeding avoidance in this species.     

Sequence-based evidence for major histocompatibility complex-disassortative mating in a colonial seabird

The major histocompatibility complex (MHC) is a polymorphic gene family associated with immune defence, and it can play a role in mate choice. Under the genetic compatibility hypothesis, females choose mates that differ genetically from their own MHC genotypes, avoiding inbreeding and/or enhancing the immunocompetence of their offspring. We tested this hypothesis of disassortative mating based on MHC genotypes in a population of great frigatebirds (Fregata minor) by sequencing the second exon of MHC class II B. Extensive haploid cloning yielded two to four alleles per individual, suggesting the amplification of two genes. MHC similarity between mates was not significantly different between pairs that did (n = 4) or did not (n = 42) exhibit extra-pair paternity. Comparing all 46 mated pairs to a distribution based on randomized re-pairings, we observed the following (i): no evidence for mate choice based on maximal or intermediate levels of MHC allele sharing (ii), significantly disassortative mating based on similarity of MHC amino acid sequences, and (iii) no evidence for mate choice based on microsatellite alleles, as measured by either allele sharing or similarity in allele size. This suggests that females choose mates that differ genetically from themselves at MHC loci, but not as an inbreeding-avoidance mechanism.     

No evidence for inbreeding avoidance in a great reed warbler population

Inbreeding depression may drive the evolution of inbreedingavoidance through dispersal and mate choice. In birds, manyspecies show female-biased dispersal, which is an effectiveinbreeding avoidance mechanism. In contrast, there is scarceevidence in birds for kin discriminative mate choice, whichmay, at least partly, reflect difficulties detecting it. First,kin discrimination may be realized as dispersal, and this isdifficult to distinguish from other causes of dispersal. Second,even within small, isolated populations, it is often difficultto determine the potential candidates available to a femalewhen choosing a mate. We sought evidence for inbreeding avoidancevia kin discrimination in a breeding population of great reedwarblers (Acrocephalus arundinaceus) studied over 17 years.Inbreeding depression is strong in the population, suggestingthat it would be adaptive to avoid relatives as mates. Detaileddata on timing of settlement and mate search movements madeit possible to identify candidate mates for each female, andlong-term pedigrees and resolved parentage enabled us to estimaterelatedness between females and their candidate mates. We foundno evidence for kin discrimination: mate choice was random withrespect to relatedness when all mate-choice events were considered,and, after correction for multiple tests, also in all breedingyears. We suggest that dispersal is a sufficient inbreedingavoidance mechanism in most situations, although the lack ofkin discriminative mate choice has negative consequences forsome females, because they end up mating with closely relatedmales that lowers their fitness.     

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.     

Are extra‐pair males different from cuckolded males? A case study and a meta‐analytic examination

Traditional models for female extra‐pair matings assume that females benefit indirectly from extra‐pair mating behaviour. Under these so‐called adaptive models, extra‐pair males are hypothesized to have more compatible genotypes, larger body size, exaggerated ornaments or to be older than cuckolded males. Alternatively, (‘nonadaptive’) models that consider female extra‐pair matings to be a by‐product posit that female extra‐pair mating can be maintained even if there is no benefit to females. This could happen if, for example, males gained fitness benefits from extra‐pair mating, while female and male extra‐pair mating behaviours were genetically correlated. Extra‐pair males are also expected to be older and larger if this improves their ability to convince or coerce females to mate. We investigated whether a female's extra‐pair mates differed from her cuckolded mate in both genetic and phenotypic traits by analysing data from an insular house sparrow population. We found that extra‐pair males were older than cuckolded males, consistent with both models. However, in contrast to the expectations from from adaptive models, extra‐pair and cuckolded males were of similar genetic relatedness, and hence expected compatibility, with the female, and had comparable body size and secondary sexual traits. We also updated previous meta‐analyses examining differences between extra‐pair and cuckolded males. The meta‐analytic results matched results from our house sparrow case study. Although we cannot completely exclude indirect benefits for females, nonadaptive models may better explain female extra‐pair matings. These neglected alternative models deserve more research attention, and this should improve our understanding of the evolution of mating systems.     

Colourful male guppies produce faster and more viable sperm

In guppies (Poecilia reticulata) precopulatory sexual selection (via female choice) and post-copulatory selection (via sperm competition) both favour males with relatively high levels of carotenoid (orange) pigmentation, suggesting that colourful males produce more competitive ejaculates. Here we test whether there is a positive association between male orange pigmentation and sperm quality. Our analysis of sperm quality focused on sperm swimming speeds (using CASA: computer-assisted sperm analysis to estimate three parameters of sperm velocity in vitro), sperm viability (proportion of live sperm per stripped ejaculate) and sperm lengths. We found that males with relatively large areas of orange pigmentation had significantly faster and more viable sperm than their less ornamented counterparts, suggesting a possible link between dietary carotenoid intake and sperm quality. By contrast, we found no relationship between sperm length (head length and total sperm length) and male phenotype. These findings, in conjunction with previous work showing that highly ornamented male guppies sire higher quality offspring, suggest that female preference for colourful males and sperm competition work in concert to favour intrinsically higher quality males.     

Secondary sexual ornamentation and non-additive genetic benefits of female mate choice

Ornamental secondary sexual traits are hypothesized to evolve in response to directional mating preferences for more ornamented mates. Such mating preferences may themselves evolve partly because ornamentation indicates an individual's additive genetic quality (good genes). While mate choice can also confer non-additive genetic benefits (compatible genes), the identity of the most 'compatible' mate is assumed to depend on the choosy individual's own genotype. It is therefore unclear how choice for non-additive genetic benefits could contribute to directional mating preferences and consequently the evolution of ornamentation. In free-living song sparrows (Melospiza melodia), individual males varied in their kinship with the female population. Furthermore, a male's song repertoire size, a secondary sexual trait, was negatively correlated with kinship such that males with larger repertoires were less closely related to the female population. After excluding close relatives as potential mates, individual females were on average less closely related to males with larger repertoires. Therefore, female song sparrows expressing directional preferences for males with larger repertoires would on average acquire relatively unrelated mates and produce relatively outbred offspring. Such non-additive genetic fitness benefits of directional mating preferences, which may reflect genetic dominance variance expressed in structured populations, should be incorporated into genetic models of sexual selection.