Sampling scale can cause bias in positive assortative mating estimates: evidence from two intertidal snails

Assortative mating in the wild is commonly estimated by correlating between traits in mating pairs (e.g. the size of males and females). Unfortunately, such an approach may suffer from considerable sampling bias when the distribution of different expressions of a trait in the wild is nonrandom (e.g. when segregation of different size classes of individuals occurs in different microhabitats or areas). Consequently, any observed trait correlation in the wild can be an artefact of pooling heterogeneous samples of mating pairs from different microhabitats or areas rather than true nonrandom matings. This bias in estimating trait correlations as a result of sampling scale is termed the scale‐of‐choice effect (SCE). In the present study, we use two intertidal littorinid species from Hong Kong to show how the SCE can bias size‐assortative mating estimates from mating pairs captured in the wild, empirically demonstrating the influence of this effect on measures of positive assortative mating. This finding cautions that studies overlooking the SCE may have misinterpreted the magnitude and the cause of assortative mating, and we provide a new analytical approach for protecting against this potential bias in future studies.     

PROBLEMS WITH TESTING INBREEDING AVOIDANCE: THE CASE OF THE COLLARED FLYCATCHER

Four year's data on collared flycatchers, Ficedula albicollis, breeding in a nestbox plot on the island of Gotland, Sweden, was used to investigate whether individuals avoid mating with close kin (i.e., parents or sibs). Only one case of close inbreeding (0.5% of all pairs) was observed during the years of study. The observed frequency of close inbreeding was compared to expected frequencies based on two different null models. Assuming no inbreeding avoidance behaviors (e.g., dispersal or kin recognition), but taking into account the fact that mortality, and different arrival and pairing times of individuals reduce the probability of mating with close kin, the expected frequency of close inbreeding is 10% and 15% for female and male recruits (i.e., born in the study plot), respectively. However, assuming mating to be random within the study plot reduced the expected frequency of close inbreeding to 1% or less for both males and females. Consequently, conclusions drawn concerning inbreeding avoidance depend on the null model used. Contrasting estimated costs of tolerating close inbreeding with those of avoiding it (by dispersal to other plots), however, suggests that the costs of avoiding close inbreeding are substantially greater than those of tolerating it. Therefore, although inbreeding avoidance cannot be rejected as a cause of dispersal of this species, it is not the primary cause, and particularly not for sex-biased dispersal. The general problems of investigating inbreeding avoidance are discussed. It is argued that all previous null models based on random mating in finite populations produce expected frequencies of close inbreeding that in fact include inbreeding avoidance, since they implicitly assume random dispersal within a finite population. Thus, comparisons between observed and expected frequencies of close inbreeding based on random mating are inadequate. The most promising method of investigating inbreeding avoidance is to experimentally study individual movements and mating preferences in the presence and absence of close kin.     

The transition to social inbred mating systems in spiders: role of inbreeding tolerance in a subsocial predecessor

The social spiders are unusual among cooperatively breeding animals in being highly inbred. In contrast, most other social organisms are outbred owing to inbreeding avoidance mechanisms. The social spiders appear to originate from solitary subsocial ancestors, implying a transition from outbreeding to inbreeding mating systems. Such a transition may be constrained by inbreeding avoidance tactics or fitness loss due to inbreeding depression. We examined whether the mating system of a subsocial spider, in a genus with three social congeners, is likely to facilitate or hinder the transition to inbreeding social systems. Populations of subsocial Stegodyphus lineatus are substructured and spiders occur in patches, which may consist of kin groups. We investigated whether male mating dispersal prevents matings within kin groups in natural populations. Approximately half of the marked males that were recovered made short moves (< 5m) and mated within their natal patch. This potential for inbreeding was counterbalanced by a relatively high proportion of immigrant males. In mating experiments, we tested whether inbreeding actually results in lower offspring fitness. Two levels of inbreeding were tested: full sibling versus non-sib matings and matings of individuals within and between naturally occurring patches of spiders. Neither full siblings nor patch mates were discriminated against as mates. Sibling matings had no effect on direct fitness traits such as fecundity, hatching success, time to hatching and survival of the offspring, but negatively affected offspring growth rates and adult body size of both males and females. Neither direct nor indirect fitness measures differed significantly between within patch and between-patch pairs. We tested the relatedness between patch mates and nonpatch mates using DNA fingerprinting (TE-AFLP). Kinship explained 30% of the genetic variation among patches, confirming that patches are often composed of kin. Overall, we found limited male dispersal, lack of kin discrimination, and tolerance to low levels of inbreeding. These results suggest a history of inbreeding which may reduce the frequency of deleterious recessive alleles in the population and promote the evolution of inbreeding tolerance. It is likely that the lack of inbreeding avoidance in subsocial predecessors has facilitated the transition to regular inbreeding social systems.     

Genetics and demography: Notes on the third Princeton conference (Princeton,N.J., October 20–22, 1966)

Abstract

A method is presented for the analysis of deviations from random mating. Kinship, demographic, social, and spatial characteristics observed among married couples have been compared with the distributions expected if mates were chosen at random from all possible pairs of mates. This procedure has been used to investigate both failure to mate and patterns of assortative mating for cohorts born on Sanday, Orkney Islands, between 1885 and 1924. Differences in mating opportunity were observed. The 315 males who eventually married on the island differed from the 446 never‐married males in birth order and sibship size as well as geographic and kinship “distances” measured between ego and all females available for marriage. Comparison of wives with the potential mates of married males indicated that mating was assortative with respect to kinship, demographic, social, and geographic characteristics. Further implications of this nonrandom pattern of mate choice are discussed and application of this method to other populations suggested.     

PARTITIONING THE EFFECTS OF SPATIAL ISOLATION,NEST HABITAT,AND INDIVIDUAL DIET IN CAUSING ASSORTATIVE MATING WITHIN A POPULATION OF THREESPINE STICKLEBACK

Assortative mating is measured as a phenotypic or genotypic correlation between mates. Although biologists typically view assortative mating in terms of mate preference for similar partners, correlations between mates can also arise from phenotypic spatial structure arising from spatial isolation or habitat preferences. Here, we test whether diet‐assortative mating within an ecologically variable population of threespine stickleback results from small‐scale geographic isolation or microhabitat preference. We find evidence for assortative mating in the form of a positive correlation between mated pairs’ diets (measured using stable isotopes). Stable isotopes reveal diet differences between different nesting areas and among individuals using different nest habitat within a nesting area. This spatial segregation of diet types should generate some assortative mating, but is insufficient to explain the observed assortment strength. Significant male–female isotope correlations remain after controlling for spatial variables. We therefore conclude that sticklebacks’ diet‐assortative mating arises from additional behavioral preference. More generally, our results illustrate the point that spatial segregation can only drive appreciable levels of phenotypic assortative mating when environment‐phenotype correlations are parallel and strong in both sexes. Consequently, intraspecific assortative mating may typically entail mating preferences rather than just spatial cosegregation of phenotypes.     

Social network analysis of mating patterns in American black bears (Ursus americanus)

Nonrandom mating can structure populations and has important implications for population‐level processes. Investigating how and why mating deviates from random is important for understanding evolutionary processes as well as informing conservation and management. Prior to the implementation of parentage analyses, understanding mating patterns in solitary, elusive species like bears was virtually impossible. Here, we capitalize on a long‐term genetic data set collected from black bears (Ursus americanus) (N = 2422) in the Northern Lower Peninsula (NLP) of Michigan, USA. We identified mated pairs using parentage analysis and applied logistic regression (selection) models that controlled for features of the social network, to quantify the effects of individual characteristics, and spatial and population demographic factors on mating dynamics. Logistic regression models revealed that black bear mating was associated with spatial proximity of mates, male age, the time a pair had coexisted, local population density and relatedness. Mated pairs were more likely to contain older males. On average, bears tended to mate with nearby individuals to whom they were related, which does not support the existence of kin recognition in black bears. Pairwise relatedness was especially high for mated pairs containing young males. Restricted dispersal and high male turnover from intensive harvest mortality of NLP black bears are probably the underlying factors associated with younger male bears mating more often with female relatives. Our findings illustrate how harvest has the potential to disrupt the social structure of game species, which warrants further attention for conservation and management.     

Population structure of the Jirels: patterns of mate choice

The influence of mating practices on genetic structure has been an area of great interest for anthropologists. In this paper, the techniques of potential mates analysis are employed to explore the mating patterns observed among the Jirels, a tribal population of eastern Nepal. Genealogical, anthropometric, dermatoglyphic, and demographic data for members of seven Jirel villages are used. Potential mate pools for a sample of 268 females are enumerated by village. Age structure and the Jirel restriction against clan endogamy are found to severely limit the number of males who are potential mates for a given female. The mating structure of the population is illuminated by statistical analysis of the characteristics of 160 actual mate pairs and all corresponding potential mate pairs. Using this approach several general mate choice practices were verified: 1) biological kin tend to be avoided as mates, 2) members of the same clan are excluded as potential mates, 3) mate exchange between clans is nonrandom, 4) individuals similar in age tend to be selected as mates, and 5) mates are drawn from the natal village more often than random expectation. A multivariate phenotypic distance measure between individuals did not reveal any evidence for assortative mating for either anthropometric or dermatoglyphic characters.     

Assortative mating and the cost of inbreeding — A simulation approach

Assortative mating is an important factor in the process of speciation. Models of speciation frequently deal with small founder populations often with mating preferences based on ecological traits or habitat preferences. Small populations, on the other hand might suffer from inbreeding. However, few studies have explored the combined effects of assortative mating and inbreeding in such populations. Can they speciate, or are they doomed to eventually go extinct? With this simulation we show that assortative mating based on similarities increases the possibility for change in a population, as long as the population does not suffer from inbreeding depression. Inbred populations seem not to be able to cope with strong assortative mating, as this is likely to elevate the level of inbreeding, increasing the risks of inbreeding depression and as a result decreasing population mean fitness. This in turn hinders the possibility of change, and instead might drive the population to extinction.     

Evidence of low within‐pair genetic relatedness in a relict population of Thorn‐tailed Rayadito despite long‐term isolation

Investigating whether mating patterns are biased in relation to kinship in isolated populations can provide a better understanding of the occurrence of inbreeding avoidance mechanisms in wild populations. Here, we report on the genetic relatedness (r) among breeding pairs in a relict population of Thorn‐tailed Rayadito (Aphrastura spinicauda) in north‐central Chile that has experienced a long‐term history of isolation. We used simulations based on 8 years of data to assess whether mating is random with respect to relatedness. We found that mean and median population values of pair relatedness tended to be lower than randomly generated values, suggesting that mating is not random with respect to kinship. We hypothesize that female‐biased dispersal is the main mechanism reducing the likelihood of mating among kin, and that the proportion of related pairs (i.e., r > 0.125) in the study population (25%) would presumably be higher in the absence of sex‐biased dispersal. The occurrence of other mechanisms such as extra‐pair copulations, delayed breeding, and active inbreeding avoidance through kin discrimination cannot be dismissed and require further study.     

To be,or not to be,related: how female guppies bias sperm usage

In the Descent of Man, Darwin wrote “the power to charm the female has sometimes been more important than the power to conquer other males in battle” (Darwin 1871 ). Since his pioneering work, the field of sexual selection has exploded as biologists strive to understand how females bias fertilization towards preferred males. In the context of genetic relatedness between potential mates, two main hypotheses exist to explain female mating preferences. First, a female may bias fertilization towards genetically dissimilar males if she gains evolutionary fitness through the production of genetically diverse offspring – a model known as dissortative mating or inbreeding avoidance. Second, a female may favour genetically similar males if her offspring are more likely to inherit coadapted gene complexes – a model known as assortative mating or outbreeding avoidance. In this issue of Molecular Ecology, Gasparini et al. (2015) demonstrate that female guppies bias fertilization towards males which are more related to them at major histocompatibility (MHC) class IIB genes. Amazingly, this bias occurs after insemination of sperm from two different males.     

Assortative mating for fitness and the evolution of recombination

To understand selection on recombination, we need to consider how linkage disequilibria develop and how recombination alters these disequilibria. Any factor that affects the development of disequilibria, including nonrandom mating, can potentially change selection on recombination. Assortative mating is known to affect linkage disequilibria but its effects on the evolution of recombination have not been previously studied. Given that assortative mating for fitness can arise indirectly via a number of biologically realistic scenarios, it is plausible that weak assortative mating occurs across a diverse set of taxa. Using a modifier model, we examine how assortative mating for fitness affects the evolution of recombination under two evolutionary scenarios: selective sweeps and mutation-selection balance. We find there is no net effect of assortative mating during a selective sweep. In contrast, assortative mating could have a large effect on recombination when deleterious alleles are maintained at mutation-selection balance but only if assortative mating is sufficiently strong. Upon considering reasonable values for the number of loci affecting fitness components, the strength of selection, and the mutation rate, we conclude that the correlation in fitness between mates is unlikely to be sufficiently high for assortative mating to affect the evolution of recombination in most species.     

ASSORTATIVE MATING AND THE ADAPTIVE LANDSCAPE

The ability of a population to shift from one adaptive peak to another was examined for a two-locus model with different degrees of assortative mating, selection, and linkage. As expected, if the proportion of the population that mates assortatively increases, so does its ability to shift to a new peak. Assortative mating affects this process by allowing the mean fitness of a population to increase monotonically as it passes through intermediate gene frequencies on the way to a new, higher, homozygotic peak. Similarly, if the height of the new peak increases or selection against intermediates becomes less severe, the population becomes more likely to shift to a new peak. Close linkage also helps the shift to a new adaptive peak and acts similarly to assortative mating, but it is not necessary for such a shift as was previously thought. When a population shifts to a new peak, the number of generations required is significantly less than that needed to return to the original peak when that happens. The short period of time required may be an explanation for rapid changes in the geological record. Under extremely high degrees of assortative mating, the shift takes longer, presumably because of the difficulty of breaking up less favored allelic combinations.     

The strength of assortative mating for flowering date and its basis in individual variation in flowering schedule

Although it has been widely asserted that plants mate assortatively by flowering time, there is virtually no published information on the strength or causes of phenological assortment in natural populations. When strong, assortative mating can accelerate the evolution of plant reproductive phenology through its inflationary effect on genetic variance. We estimated potential assortative mating for flowering date in 31 old‐field species in Ontario, Canada. For each species, we constructed a matrix of pairwise mating probabilities from the individual flowering schedules, that is the number of flower deployed on successive dates. The matrix was used to estimate the phenotypic correlation between mates, ρ, for flowering date. We also developed a measure of flowering synchrony within species, S, based upon the eigenstructure of the mating matrix. The mean correlation between pollen recipients and potential donors for flowering date was  = 0.31 (range: 0.05–0.63). A strong potential for assortative mating was found among species with high variance in flowering date, flowering schedules of short duration and skew towards early flower deployment. Flowering synchrony, S, was negatively correlated with potential assortment (r = ?0.49), but we go on to show that although low synchrony is a necessary condition for phenological assortative mating, it may not be sufficient to induce assortment for a given phenological trait. The potential correlation between mates showed no seasonal trend; thus, as climate change imposes selection on phenology through longer growing seasons, spring‐flowering species are no more likely to experience an accelerated evolutionary response than summer species.     

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.     

How Pronghorn Females Avoid Inbreeding Depression

After a bottleneck in a closed population of pronghorn (Antilocapra americana), some inbred matings occurred, and we detected significant inbreeding depression. But inbred matings occurred less frequently than would be expected by chance. Pronghorn females chose mates after a sampling period and had complete control of the mating decision. Therefore, to discover the behavioral mechanism by which females avoided mating with close kin, we studied female movements and courtship sequences. When females moved from one harem to another in the sampling process, they did not shift to harem males of lower coancestry as they approached estrus. Rather, females progressed more slowly through the later courtship stages when the harem male was related vs. unrelated. Also, the rates of male courtship acts were higher within unrelated vs. related pairs. Some females appeared to use multiple mating as an inbreeding avoidance strategy. Our results suggested that inbreeding avoidance by female pronghorn occurred primarily by reactions to the late stages of male courtship, rather than by spatial avoidance of related males.     

MHC class II‐assortative mate choice in European badgers (Meles meles)

The major histocompatibility complex (MHC) plays a crucial role in the immune system, and in some species, it is a target by which individuals choose mates to optimize the fitness of their offspring, potentially mediated by olfactory cues. Under the genetic compatibility hypothesis, individuals are predicted to choose mates with compatible MHC alleles, to increase the fitness of their offspring. Studies of MHC‐based mate choice in wild mammals are under‐represented currently, and few investigate more than one class of MHC genes. We investigated mate choice based on the compatibility of MHC class I and II genes in a wild population of European badgers (Meles meles). We also investigated mate choice based on microsatellite‐derived pairwise relatedness, to attempt to distinguish MHC‐specific effects from genomewide effects. We found MHC‐assortative mating, based on MHC class II, but not class I genes. Parent pairs had smaller MHC class II DRB amino acid distances and smaller functional distances than expected from random pairings. When we separated the analyses into within‐group and neighbouring‐group parent pairs, only neighbouring‐group pairs showed MHC‐assortative mating, due to similarity at MHC class II loci. Our randomizations showed no evidence of genomewide‐based inbreeding, based on 35 microsatellite loci; MHC class II similarity was therefore the apparent target of mate choice. We propose that MHC‐assortative mate choice may be a local adaptation to endemic pathogens, and this assortative mate choice may have contributed to the low MHC genetic diversity in this population.     

Kin encounter rate and inbreeding avoidance in canids

Mating with close kin can lead to inbreeding depression through the expression of recessive deleterious alleles and loss of heterozygosity. Mate selection may be affected by kin encounter rate, and inbreeding avoidance may not be uniform but associated with age and social system. Specifically, selection for kin recognition and inbreeding avoidance may be more developed in species that live in family groups or breed cooperatively. To test this hypothesis, we compared kin encounter rate and the proportion of related breeding pairs in noninbred and highly inbred canid populations. The chance of randomly encountering a full sib ranged between 1-8% and 20-22% in noninbred and inbred canid populations, respectively. We show that regardless of encounter rate, outside natal groups mates were selected independent of relatedness. Within natal groups, there was a significant avoidance of mating with a relative. Lack of discrimination against mating with close relatives outside packs suggests that the rate of inbreeding in canids is related to the proximity of close relatives, which could explain the high degree of inbreeding depression observed in some populations. The idea that kin encounter rate and social organization can explain the lack of inbreeding avoidance in some species is intriguing and may have implications for the management of populations at risk.     

Banded mongooses avoid inbreeding when mating with members of the same natal group

Inbreeding and inbreeding avoidance are key factors in the evolution of animal societies, influencing dispersal and reproductive strategies which can affect relatedness structure and helping behaviours. In cooperative breeding systems, individuals typically avoid inbreeding through reproductive restraint and/or dispersing to breed outside their natal group. However, where groups contain multiple potential mates of varying relatedness, strategies of kin recognition and mate choice may be favoured. Here, we investigate male mate choice and female control of paternity in the banded mongoose (Mungos mungo), a cooperatively breeding mammal where both sexes are often philopatric and mating between relatives is known to occur. We find evidence suggestive of inbreeding depression in banded mongooses, indicating a benefit to avoiding breeding with relatives. Successfully breeding pairs were less related than expected under random mating, which appeared to be driven by both male choice and female control of paternity. Male banded mongooses actively guard females to gain access to mating opportunities, and this guarding behaviour is preferentially directed towards less closely related females. Guard–female relatedness did not affect the guard's probability of gaining reproductive success. However, where mate‐guards are unsuccessful, they lose paternity to males that are less related to the females than themselves. Together, our results suggest that both sexes of banded mongoose use kin discrimination to avoid inbreeding. Although this strategy appears to be rare among cooperative breeders, it may be more prominent in species where relatedness to potential mates is variable, and/or where opportunities for dispersal and mating outside of the group are limited.     

Assortative mating by size: A meta-analysis of mating patterns in water striders

Summary Assortative mating by size is a common mating pattern that can be generated by several different behavioural mechanisms, with different evolutionary implications. Assortative mating is typically associated with sexual selection and has been regarded as an attribute of populations, species, mating systems or even higher order taxa. In most animal groups, however, appropriate analyses of assortative mating at these different levels are lacking and the causes and forms of assortative mating are poorly understood. Here, we analyse 45 different population level estimates of assortative mating and non-random mating by size in seven confamiliar species of water striders that share a common mating system. A hierarchical comparative analysis shows that virtually all the variance within the clade occurs among samples within species. We then employ meta-analysis to estimate the overall strength of assortative mating, to determine the form of assortative mating and to further assess potential differences among species as well as the probable causes of assortative mating in this group of insects. We found overall weak but highly significant positive assortative mating. We show that analyses of the degree of heteroscedasticity in plots of male versus female size are critical, since the evolutionary implications of true and apparent assortative mating differ widely and conclude that the positive assortative mating observed in water striders was of the true rather than the apparent form. Further, within samples, mating individuals were significantly larger than non-mating individuals in both males and females. All of these non-random mating patterns were consistent among species and we conclude that weak positive assortative mating by size is a general characteristic of those water strider species that share this mating system. We use our results to illustrate the importance of distinguishing between different forms of assortative mating, to discriminate between various behavioural causes of assortative mating and to assess potential sources of interpopulational variance in estimates of assortative mating. Finally, we discuss the value of using meta-analytic techniques for detecting overall patterns in multiple studies of non-random mating.     

Immigration prevents inbreeding in a growing colony of a long‐lived and philopatric seabird

Mating between close relatives can have deleterious effects on reproductive success or offspring fitness, which should favour the evolution of active or passive inbreeding avoidance mechanisms. In birds, evidence for active inbreeding avoidance by kin‐discriminative mate choice is scarce; many studies describe random mating in relation to kinship and thus support passive inbreeding avoidance by natal dispersal. However, most studies were conducted in island populations of short‐lived passerines with fast alternation of generations. In this study, we present inbreeding estimates based on pedigree data from a 16‐year study in a coastal colony of Common Terns Sterna hirundo, a long‐lived seabird with delayed sexual maturation and low rates of extra‐pair paternity. Incestuous mating was rare (four of 2387 pairs), even if partially accounting for incomplete pedigrees. Although the average relatedness of observed pairs was lower than would be expected from random pairing, the inbreeding coefficient did not differ from random mating. Hence, we found no clear evidence for active inbreeding avoidance by kin‐discriminative mate choice, and the low level of inbreeding seems to be related to the high immigration rate in the colony and thus to be maintained passively by dispersal.