Evidence that pairing with genetically similar mates is maladaptive in a monogamous bird

Background  

Evidence of multiple genetic criteria of mate choice is accumulating in numerous taxa. In many species, females have been shown to pair with genetically dissimilar mates or with extra-pair partners that are more genetically compatible than their social mates, thereby increasing their offsprings' heterozygosity which often correlates with offspring fitness. While most studies have focused on genetically promiscuous species, few studies have addressed genetically monogamous species, in which mate choice tends to be mutual.     

How Do Females’ Genetic Characteristics Influence Male Mate Preference in the Terrestrial Isopod Armadillidium vulgare?

Genetic diversity is a key factor that can influence mate choice in many species. We experimentally determined the influence of this factor on mate preference in the crustacean terrestrial isopod Armadillidium vulgare. This biological model is gregarious which could increase the risk of inbreeding by mating with closely related partners. Mechanisms of inbreeding avoidance during mate choice can thus be expected. Moreover, previous studies predict that males would be the choosy sex. We performed Y‐choice tests giving males the choice between two females presenting different levels of heterozygosity and genetic similarity to the male. Our results show potential inbreeding avoidance according to the genetic characteristics of females presented to males. The higher the variation in genetic similarity to the male between females is, the higher the preference of the male towards the most dissimilar female is. Hence, male preferences may only be detectable when the difference between females’ genetic characteristics is large enough. If heterozygosity is associated with fitness in A. vulgare (as in many organisms), the patterns of mate preference we observe may be adaptive.     

MHC‐disassortative mate choice and inbreeding avoidance in a solitary primate

Sexual selection theory suggests that choice for partners carrying dissimilar genes at the major histocompatibility complex (MHC) may play a role in maintaining genetic variation in animal populations by limiting inbreeding or improving the immunity of future offspring. However, it is often difficult to establish whether the observed MHC dissimilarity among mates drives mate choice or represents a by‐product of inbreeding avoidance based on MHC‐independent cues. Here, we used 454‐sequencing and a 10‐year study of wild grey mouse lemurs (Microcebus murinus), small, solitary primates from western Madagascar, to compare the relative importance on the mate choice of two MHC class II genes, DRB and DQB, that are equally variable but display contrasting patterns of selection at the molecular level, with DRB under stronger diversifying selection. We further assessed the effect of the genetic relatedness and of the spatial distance among candidate mates on the detection of MHC‐dependent mate choice. Our results reveal inbreeding avoidance, along with disassortative mate choice at DRB, but not at DQB. DRB‐disassortative mate choice remains detectable after excluding all related dyads (characterized by a relatedness coefficient r > 0), but varies slightly with the spatial distance among candidate mates. These findings suggest that the observed deviations from random mate choice at MHC are driven by functionally important MHC genes (like DRB) rather than passively resulting from inbreeding avoidance and further emphasize the need for taking into account the spatial and genetic structure of the population in correlative tests of MHC‐dependent mate choice.     

Female mating preferences and offspring survival: testing hypotheses on the genetic basis of mate choice in a wild lekking bird

Indirect benefits of mate choice result from increased offspring genetic quality and may be important drivers of female behaviour. ‘Good‐genes‐for‐viability’ models predict that females prefer mates of high additive genetic value, such that offspring survival should correlate with male attractiveness. Mate choice may also vary with genetic diversity (e.g. heterozygosity) or compatibility (e.g. relatedness), where the female's genotype influences choice. The relative importance of these nonexclusive hypotheses remains unclear. Leks offer an excellent opportunity to test their predictions, because lekking males provide no material benefits and choice is relatively unconstrained by social limitations. Using 12 years of data on lekking lance‐tailed manakins, Chiroxiphia lanceolata, we tested whether offspring survival correlated with patterns of mate choice. Offspring recruitment weakly increased with father attractiveness (measured as reproductive success, RS), suggesting attractive males provide, if anything, only minor benefits via offspring viability. Both male RS and offspring survival until fledging increased with male heterozygosity. However, despite parent–offspring correlation in heterozygosity, offspring survival was unrelated to its own or maternal heterozygosity or to parental relatedness, suggesting survival was not enhanced by heterozygosity per se. Instead, offspring survival benefits may reflect inheritance of specific alleles or nongenetic effects. Although inbreeding depression in male RS should select for inbreeding avoidance, mates were not less related than expected under random mating. Although mate heterozygosity and relatedness were correlated, selection on mate choice for heterozygosity appeared stronger than that for relatedness and may be the primary mechanism maintaining genetic variation in this system despite directional sexual selection.     

An integrative mating system assessment of a nonmodel,economically important Pacific rockfish (Sebastes melanops) reveals nonterritorial polygamy and conservation implications for a large species flock

Characterizing the mating systems of long‐lived, economically important Pacific rockfishes comprising the viviparous Sebastes species flock is crucial for their conservation. However, direct assignment of mating success to sires is precluded by open, offshore populations and high female fecundity. We addressed this challenge by integrating paternity‐assigned mating success of females with the adult sex ratio (ASR) of the population, male evolutionary responses to receptive females, and reproductive life history traits—in the framework of sexual selection theory—to assess the mating system of Sebastes melanops. Microsatellite parentage analysis of 17 pregnant females, 1,256 of their progeny, and 106 adults from the population yielded one to four sires per brood, a mean of two sires, and a female mate frequency distribution with a truncated normal (random) pattern. The 11 multiple paternity broods all contained higher median allele richness than the six single paternity broods (Wilcoxon test: W = 0, p < .001), despite similar levels of average heterozygosity. By sampling sperm and alleles from different males, polyandrous females gain opportunities to enhance their sperm supply and to lower the cost of mating with genetically incompatible males through reproductive compensation. A mean of two mates per mated female with a variance of one, an ASR = 1.2 females per male, and the expected population mean of 2.4 mates for mated males (and the estimated 35 unavailable sires), fits polygamous male mate frequency distributions that distinguish polygynandry and polyandrogyny mating systems, that is, variations of polygamy, but not polyandry. Inference for polygamy is consistent with weak premating sexual selection on males, expected in mid‐water, schooling S. melanops, owing to polyandrous mating, moderately aggregated receptive females, an even ASR, and no territories and nests used for reproduction. Each of these characteristics facilitates more mating males and erodes conspicuous sexual dimorphism. Evaluation of male evolutionary responses of demersal congeners that express reproductively territorial behavior revealed they have more potential mechanisms for producing premating sexual selection, greater variation in reproductive success, and a reduced breeding effective population size of adults and annual effective size of a cohort, compared to S. melanops modeled with two mates per adult. Such divergence in behavior and mating system by territorial species may differentially lower their per capita birth rates, subsequent population growth, and slow their recovery from exploitation.     

MHC,mate choice and heterozygote advantage in a wild social primate

Preferences for mates carrying dissimilar genes at the major histocompatibility complex (MHC) may help animals increase offspring pathogen resistance or avoid inbreeding. Such preferences have been reported across a range of vertebrates, but have rarely been investigated in social species other than humans. We investigated mate choice and MHC dynamics in wild baboons (Papio ursinus). MHC Class II DRB genes and 16 microsatellite loci were genotyped across six groups (199 individuals). Based on the survey of a key segment of the gene‐rich MHC, we found no evidence of mate choice for MHC dissimilarity, diversity or rare MHC genotypes. First, MHC dissimilarity did not differ from random expectation either between parents of the same offspring or between immigrant males and females from the same troop. Second, female reproductive success was not influenced by MHC diversity or genotype frequency. Third, population genetic structure analysis revealed equally high genotypic differentiation among troops, and comparable excess heterozygosity within troops for juveniles, at both Mhc‐DRB and neutral loci. Nevertheless, the age structure of Mhc‐DRB heterozygosity suggested higher longevity for heterozygotes, which should favour preferences for MHC dissimilarity. We propose that high levels of within‐group outbreeding, resulting from group‐living and sex‐biased dispersal, might weaken selection for MHC‐disassortative mate choice.     

Genetic diversity of North American captive‐born gorillas (Gorilla gorilla gorilla)

Western lowland gorillas (Gorilla gorilla gorilla) are designated as critically endangered and wild populations are dramatically declining as a result of habitat destruction, fragmentation, diseases (e.g., Ebola) and the illegal bushmeat trade. As wild populations continue to decline, the genetic management of the North American captive western lowland gorilla population will be an important component of the long‐term conservation of the species. We genotyped 26 individuals from the North American captive gorilla collection at 11 autosomal microsatellite loci in order to compare levels of genetic diversity to wild populations, investigate genetic signatures of a population bottleneck and identify the genetic structure of the captive‐born population. Captive gorillas had significantly higher levels of allelic diversity (t₇ = 4.49, P = 0.002) and heterozygosity (t₇ = 4.15, P = 0.004) than comparative wild populations, yet the population has lost significant allelic diversity while in captivity when compared to founders (t₇ = 2.44, P = 0.04). Analyses suggested no genetic evidence for a population bottleneck of the captive population. Genetic structure results supported the management of North American captive gorillas as a single population. Our results highlight the utility of genetic management approaches for endangered nonhuman primate species.     

The mating game: do opposites really attract?

When selecting a mate, females of many species face a complicated decision: choosing a very closely related mate will lead to inbreeding, while choosing a mate who is too genetically dissimilar risks breaking up beneficial gene complexes or local genetic adaptations. To ensure the best genetic quality of their offspring, the perfect compromise lies somewhere in between: an optimally genetically dissimilar partner. Empirical evidence demonstrating female preference for genetically dissimilar mates is proof of the adage 'opposites attract'. In stark contrast, Chandler & Zamudio (2008) show in this issue of Molecular Ecology that female spotted salamanders often choose males that are genetically more similar to themselves (although not if the males are small). Along with other recent work, these field studies highlight the broad spectrum of options available to females with respect to relatedness in their choice of mate that belies this rule of thumb.     

Confrontation of cryptic diversity and mate discrimination within Gammarus pulex and Gammarus fossarum species complexes

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Microsatellite loci for the basal angiosperm Austrobaileya scandens (Austrobaileyaceae)

We developed nine microsatellite loci for the basal angiosperm Austrobaileya scandens, a vine endemic to northeastern Australia. High levels of polymorphism were detected in 30 individuals from a single population, with an average of 14.78 alleles per locus and an average expected heterozygosity of 0.81. Historical inbreeding levels were significantly different from zero (f = 0.136), consistent with genetic evidence for self‐parentage in open‐pollinated progeny. The high exclusionary power of these loci (> 99.98%) indicates they will be useful in future parentage analyses designed to explore mechanisms of mate choice in Austrobaileya.     

Temporal variation of heterozygosity‐based assortative mating and related benefits in a lesser kestrel population

Heterozygosity as a target of mate choice has received much attention in recent years and there is growing evidence supporting its role in the evolution of mate preferences. In this study we analyse mating patterns in relation to heterozygosity in a lesser kestrel (Falco naumanni) population intensively monitored over six study years (2002–2007). The magnitude of heterozygosity‐based assortative mating varied over time, being particularly patent in the last study years (2006, 2007). We have found evidence that this mating pattern entails both direct and indirect‐genetic benefits. Clutch size increased with female heterozygosity and more heterozygous males raised a higher number of fledglings particularly in those years when the strength of the heterozygosity‐based assortative mating was markedly higher. In the last study year, parent–offspring correlation of heterozygosity was stronger and higher than the expected if individuals would have randomly mated with respect to heterozygosity. Overall, our results offer empirical support to the heterozygous mate hypothesis of sexual selection but suggest that genetic diversity may act as a temporally variable target for mate choice.     

TESTING SEX RATIO THEORY WITH THE MALARIA PARASITE PLASMODIUM MEXICANUM IN NATURAL AND EXPERIMENTAL INFECTIONS

The malaria parasite (Plasmodium) life history accords well with the assumptions of local mate competition (LMC) of sex ratio theory. Within a single meal of the blood‐feeding vector, sexually dimorphic gametocyte cells produce gametes (females produce one, males several) that mate and undergo sexual recombination. The theory posits several factors drive the Plasmodium sex ratio: male fecundity (gametes/male gametocyte), number and relative abundance of parasite clones, and gametocyte density. We measured these traits for the lizard malaria parasite, Plasmodium mexicanum, with a large sample of natural infections and infections from experiments that manipulated clonal diversity. Sex ratio in single‐clone infections was slightly female‐biased, but matched predictions of theory for this low‐fecundity species. Sex ratio was less female‐biased in clonally diverse infections as predicted by LMC for the experimental, but not natural infections. Gametocyte density was not positively related to sex ratio. These results are explained by the P. mexicanum life history of naturally low clonal diversity and high gametocyte production. This is the first study of a natural malaria system that examines all traits relevant to LMC in individual vertebrate hosts and suggests a striking example of sex ratio theory having significance for human public health.     

Extra‐group mating increases inbreeding risk in a cooperatively breeding bird

In many cooperatively breeding species, females mate extra‐group, the adaptive value of which remains poorly understood. One hypothesis posits that females employ extra‐group mating to access mates whose genotypes are more dissimilar to their own than their social mates, so as to increase offspring heterozygosity. We test this hypothesis using life history and genetic data from 36 cooperatively breeding white‐browed sparrow weaver (Plocepasser mahali) groups. Contrary to prediction, a dominant female's relatedness to her social mate did not drive extra‐group mating decisions and, moreover, extra‐group mating females were significantly more related to their extra‐group sires than their social mates. Instead, dominant females were substantially more likely to mate extra‐group when paired to a dominant male of low heterozygosity, and their extra‐group mates (typically dominants themselves) were significantly more heterozygous than the males they cuckolded. The combined effects of mating with extra‐group males of closer relatedness, but higher heterozygosity resulted in extra‐group‐sired offspring that were no more heterozygous than their within‐group‐sired half‐siblings. Our findings are consistent with a role for male–male competition in driving extra‐group mating and suggest that the local kin structure typical of cooperative breeders could counter potential benefits to females of mating extra‐group by exposing them to a risk of inbreeding.     

Heterozygosity-based assortative mating in blue tits (Cyanistes caeruleus): implications for the evolution of mate choice

The general hypothesis of mate choice based on non-additive genetic traits suggests that individuals would gain important benefits by choosing genetically dissimilar mates (compatible mate hypothesis) and/or more heterozygous mates (heterozygous mate hypothesis). In this study, we test these hypotheses in a socially monogamous bird, the blue tit (Cyanistes caeruleus). We found no evidence for a relatedness-based mating pattern, but heterozygosity was positively correlated between social mates, suggesting that blue tits may base their mating preferences on partner''s heterozygosity. We found evidence that the observed heterozygosity-based assortative mating could be maintained by both direct and indirect benefits. Heterozygosity reflected individual quality in both sexes: egg production and quality increased with female heterozygosity while more heterozygous males showed higher feeding rates during the brood-rearing period. Further, estimated offspring heterozygosity correlated with both paternal and maternal heterozygosity, suggesting that mating with heterozygous individuals can increase offspring genetic quality. Finally, plumage crown coloration was associated with male heterozygosity, and this could explain unanimous mate preferences for highly heterozygous and more ornamented individuals. Overall, this study suggests that non-additive genetic traits may play an important role in the evolution of mating preferences and offers empirical support to the resolution of the lek paradox from the perspective of the heterozygous mate hypothesis.     

The inbreeding strategy of a solitary primate,Microcebus murinus

Inbreeding depression may be common in nature, reflecting either the failure of inbreeding avoidance strategies or inbreeding tolerance when avoidance is costly. The combined assessment of inbreeding risk, avoidance and depression is therefore fundamental to evaluate the inbreeding strategy of a population, that is how individuals respond to the risk of inbreeding. Here, we use the demographic and genetic monitoring of 10 generations of wild grey mouse lemurs (Microcebus murinus), small primates from Madagascar with overlapping generations, to examine their inbreeding strategy. Grey mouse lemurs have retained ancestral mammalian traits, including solitary lifestyle, polygynandry and male‐biased dispersal, and may therefore offer a representative example of the inbreeding strategy of solitary mammals. The occurrence of close kin among candidate mates was frequent in young females (~37%, most often the father) and uncommon in young males (~6%) due to male‐biased dispersal. However, close kin consistently represented a tiny fraction of candidate mates (< 1%) across age and sex categories. Mating biases favouring partners with intermediate relatedness were detectable in yearling females and adult males, possibly partly caused by avoidance of daughter–father matings. Finally, inbreeding depression, assessed as the effect of heterozygosity on survival, was undetectable using a capture–mark–recapture study. Overall, these results indicate that sex‐biased dispersal is a primary inbreeding avoidance mechanism at the population level, and mating biases represent an additional strategy that may mitigate residual inbreeding costs at the individual level. Combined, these mechanisms explain the rarity of inbreeding and the lack of detectable inbreeding depression in this large, genetically diverse population.     

Effect of the Aegean Sea barrier between Europe and Asia on differentiation in Juniperus drupacea (Cupressaceae)

Juniperus drupacea is an eastern Mediterranean mountain tree with a disjunct geographical range. We hypothesized that this disjunct occurrence (the Peloponnese in Europe and the Taurus and Lebanon Mountains in Asia) should be reflected in the patterns of genetic and morphological diversity and differentiation. Nuclear microsatellite markers (nSSR) and biometric variables of the cones and seeds were examined on material sampled from four populations in Europe and eight in Asia. The Asian populations were characterized by a higher level of genetic diversity than the European populations. The genetic differentiation among populations was moderate but significant (F_ST = 0.101, P < 0.001). According to the clustering performed with BAPS, six genetically and geographically groups of populations were found: I and II from the Peloponnese; III from the Taurus Mountains; IV and V from the Anti‐Taurus Mountains; and VI from the Lebanon Mountains. The level of genetic differentiation among these six groups (4.30%, P = 0.012) probably reflects long‐lasting genetic isolation during the Pleistocene, as limited genetic admixture was found. In accordance with genetic analysis, the biometric investigations indicated a high level of morphological divergence between the European and Asian populations of the species, with further differentiation between the populations from the Taurus and Lebanon Mountains.     

Non‐timber Forest Product Harvest does not Affect the Genetic Diversity of a Tropical Tree Despite Negative Effects on Population Fitness

The level of genetic diversity in a population can affect ecological processes and plant responses to disturbance. In turn, disturbance can alter population genetic diversity and structure. Populations in fragmented and logged habitats often show reduced genetic diversity and increased inbreeding and differentiation. Long‐term harvesting of wild plants (for foliage, bark, and roots), can affect population genetic diversity by altering individual fitness and genetic contribution. Our understanding of these changes in genetic diversity due to the harvesting of plant organs is still limited. We used nine microsatellite markers to study the effect of long‐term bark and foliage harvest by Fulani people on the genetic diversity and structure of 12 populations of African mahogany (Khaya senegalensis) in Benin. We sampled 20 individuals in each population to test the effect of harvesting. For each population, we divided the samples equally between seedling and adults to test if the effects are stronger in seedlings. We found moderate genetic diversity (H_e = 0.53 ± 0.04) and weak but significant differentiation among local populations (F_ST = 0.043, P < 0.001). There was no significant effect of harvest on genetic diversity or structure, although previous work found significant negative effects of harvest on the reproduction of adults, offspring density, and population fitness. Our results suggest that demographic responses to disturbance precede a detectable genetic response. Future studies should focus on using parentage analysis to test if genotypes of harvested parents are directly represented in the offspring populations.     

Neighbouring‐group composition and within‐group relatedness drive extra‐group paternity rate in the European badger (Meles meles)

Extra‐group paternity (EGP) occurs commonly among group‐living mammals and plays an important role in mating systems and the dynamics of sexual selection; however, socio‐ecological and genetic correlates of EGP have been underexplored. We use 23 years of demographic and genetic data from a high‐density European badger (Meles meles) population, to investigate the relationship between the rate of EGP in litters and mate availability, mate incompatibility and mate quality (heterozygosity). Relatedness between within‐group assigned mothers and candidate fathers had a negative quadratic effect on EGP, whereas the number of neighbouring‐group candidate fathers had a linear positive effect. We detected no effect of mean or maximum heterozygosity of within‐group candidate fathers on EGP. Consequently, EGP was associated primarily with mate availability, subject to within‐group genetic effects, potentially to mitigate mate incompatibility and inbreeding. In badgers, cryptic female choice, facilitated by superfecundation, superfoetation and delayed implantation, prevents males from monopolizing within‐group females. This resonates with a meta‐analysis in group‐living mammals, which proposed that higher rates of EGP occur when within‐group males cannot monopolize within‐group females. In contrast to the positive meta‐analytic association, however, we found that EGP associated negatively with the number of within‐group assigned mothers and the number of within‐group candidate fathers; potentially a strategy to counter within‐group males committing infanticide. The relationship between the rate of EGP and socio‐ecological or genetic factors can therefore be intricate, and the potential for cryptic female choice must be accounted for in comparative studies.     

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.     

Disentangling the effects of breakdown of self-incompatibility and transition to selfing in North American Arabidopsis lyrata

A breakdown of self‐incompatibility (SI) followed by a shift to selfing is commonly observed in the evolution of flowering plants. Both are expected to reduce the levels of heterozygosity and genetic diversity. However, breakdown of SI should most strongly affect the region of the SI locus (S‐locus) because of the relaxation of balancing selection that operates on a functional S‐locus, and a potential selective sweep. In contrast, a transition to selfing should affect the whole genome. We set out to disentangle the effects of breakdown of SI and transition to selfing on the level and distribution of genetic diversity in North American populations of Arabidopsis lyrata. Specifically, we compared sequence diversity of loci linked and unlinked to the S‐locus for populations ranging from complete selfing to fully outcrossing. Regardless of linkage to the S‐locus, heterozygosity and genetic diversity increased with population outcrossing rate. High heterozygosity of self‐compatible individuals in outcrossing populations suggests that SI is not the only factor preventing the evolution of self‐fertilization in those populations. There was a strong loss of diversity in selfing populations, which was more pronounced at the S‐locus. In addition, selfing populations showed an accumulation of derived mutations at the S‐locus. Our results provide evidence that beyond the genome‐wide consequences of the population bottleneck associated with the shift to selfing, the S‐locus of A. lyrata shows a specific signal either reflecting the relaxation of balancing selection or positive selection.