Unrelated Mates Research Articles

Ramifications of reproductive diseases on the recovery of the Sumatran Rhinoceros Dicerorhinus sumatrensis (Mammalia: Perissodactyla: Rhinocerotidae)

The Sumatran Rhinoceros Dicerorhinus sumatrensis is on the edge of extinction. The decline of this species was initially attributed to poaching and habitat loss, but evidence presented here indicates that reproductive failure has also been a significant cause of loss, and continues to affect wild populations. Indonesia’s remaining populations of Sumatran Rhino are small and scattered, with limited access to breeding opportunities with unrelated mates. This leaves them subject to inbreeding and isolation-induced infertility, linked to fertility problems analyzed here. Sumatran Rhino females in captivity showed high rates (>70%) of reproductive pathology and/or problems with conception, which has significantly hindered the breeding program. Technological advances enabling examination immediately after capture revealed similarly high rates and types of reproductive problems in individuals from wild populations. The last seven Sumatran Rhino females captured were from areas with small declining populations, and six had reproductive problems. Going forward, capturing similarly compromised animals will take up valuable space and resources needed for fertile animals. The high risk of infertility and difficulty of treating underlying conditions, coupled with the decreasing number of remaining animals, means that the success of efforts to build a viable captive population will depend upon utilizing fertile animals and applying assisted reproductive techniques. Decades of exhaustive in situ surveys have not provided information relevant to population management or to ascertaining the fertility status of individual animals. Thus the first priority should be the capture of individuals as new founders from areas with the highest likelihood of containing fertile rhinos, indicated by recent camera trap photos of mothers with offspring. In Sumatra these areas include Way Kambas and parts of the Leuser ecosystem.

Group size and social status affect scent marking in dispersing female meerkats

Abstract Many animal species use scent marks such as feces, urine, and glandular secretions to find mates, advertise their reproductive status, and defend an exclusive territory. Scent marking may be particularly important during dispersal, when individuals emigrate from their natal territory searching for mates and a new territory to settle and reproduce. In this study, we investigated the scent-marking behavior of 30 dispersing female meerkats (Suricata suricatta) during the three consecutive stages of dispersal—emigration, transience, and settlement. We expected marking patterns to differ between dispersal stages, depending on social circumstances such as presence of unrelated mates and social status of the individuals within each dispersing coalition and also to be influenced by water and food availability. We showed that defecation probability increased with group size during the settlement stage, when newly formed groups are expected to signal their presence to other resident groups. Urination probability was higher in subordinate than in dominant individuals during each of the three dispersal stages and it decreased overall as the dispersal process progressed. Urine may, thus, be linked to advertisement of the social status within a coalition. Anal marking probability did not change across dispersal stages but increased with the presence of unrelated males and was higher in dominants than in subordinates. We did not detect any effect of rain or foraging success on defecation and urination probability. Our results suggest that feces, urine, and anal markings serve different communication purposes (e.g., within and between-group communication) during the dispersal process.

Preference for Outbreeding in Inbred Littledale’s Whistling Rats Parotomys littledalei

Inbreeding is sometimes tolerated in species occupying patchy, unpredictable habitats, when it becomes too costly to outbreed. Although traits leading to inbreeding depression may be selected against, the accumulation of deleterious alleles from constant inbreeding might promote outbreeding. Littledale’s whistling rat Parotomys littledalei occupies patchy habitats in arid western South Africa, and inbreeds in captivity without suffering inbreeding depression. We tested whether female whistling rats make different mate choice decisions based on their inbreeding status, by providing inbred and outbred females with male odours in four pairwise combinations: unrelated outbred (r = 0) versus either familiar littermate sibling (r = 0.5), half-sibling (r = 0.25), first cousin (r = 0.125), or unrelated inbred (r = 0). Inbred females generally preferred unrelated males, but did not show a preference between unrelated males and first cousins. In contrast, outbred females did not generally show a preference, but preferred first cousins to unrelated males. In breeding trials, reproductive success (output and viability of young) of outbred females paired with unrelated or related males was equally high, whereas inbred females suffered reduced reproductive success when paired with closely-related males. Our results indicate that the inbreeding status of female whistling rats influences their decision to outbreed or inbreed, which might influence their fitness. While outbred whistling rats do not suffer inbreeding depression, the costs of constant inbreeding could promote outbreeding by inbred females. We propose that the choice to inbreed or outbreed in female whistling rats depends on their inbreeding status and the genetic relatedness of available mates, with outbreeding more likely to occur unless unrelated mates are not available.

Outbreeding avoidance as probable driver of mate choice in the Asiatic toad

AbstractAcross taxa, females are routinely choosier than males in selecting mates. Several hypotheses have been advanced to explain genetic benefits behind female strategies. The inbreeding avoidance hypothesis suggests that females avoid mating with close relatives, thereby avoiding the matchup of deleterious recessive alleles. Outbreeding avoidance hypothesis suggests that females should not mate with too distantly related individuals so as to avoid the breakup of coadapted gene complexes. Although previous studies have suggested that selection should favor individuals that optimize the balance between inbreeding and outbreeding, detailed research is necessary to document the trade‐off between them and variability in mate choice across a gradient of inbreeding levels among populations. The good genes and the genetic compatibility hypotheses predict that females choose mates according to costly traits and genetic dissimilarity, respectively. Thus, to document inbreeding or outbreeding depressions and assess the contributions of mate choice based upon good genes versus genetic compatibility, we examined egg production, collected body length measurements and genotyped five microsatellite markers in six populations of Asiatic toad (Bufo gargarizans). Our results revealed that the incidence of inbreeding was higher than that expected under the assumption of random mating and relatedness between mated individuals increased when the average inbreeding level increased among populations. Our findings did not support the good genes or the genetic compatibility hypotheses. Although some other processes could have influences on mate choice of Asiatic toad and need to be tested, our results indicated that, in small and isolated toad populations, the limited availability and high cost of obtaining unrelated mates may promote outbreeding avoidance and adaptation to inbreeding to be the critical drives of female mate choice.

Postcopulatory selection for dissimilar gametes maintains heterozygosity in the endangered North Atlantic right whale

Although small populations are expected to lose genetic diversity through genetic drift and inbreeding, a number of mechanisms exist that could minimize this genetic decline. Examples include mate choice for unrelated mates and fertilization patterns biased toward genetically dissimilar gametes. Both processes have been widely documented, but the long-term implications have received little attention. Here, we combined over 25 years of field data with high-resolution genetic data to assess the long-term impacts of biased fertilization patterns in the endangered North Atlantic right whale. Offspring have higher levels of microsatellite heterozygosity than expected from this gene pool (effect size = 0.326, P < 0.011). This pattern is not due to precopulatory mate choice for genetically dissimilar mates (P < 0.600), but instead results from postcopulatory selection for gametes that are genetically dissimilar (effect size = 0.37, P < 0.003). The long-term implication is that heterozygosity has slowly increased in calves born throughout the study period, as opposed to the slight decline that was expected. Therefore, this mechanism represents a natural means through which small populations can mitigate the loss of genetic diversity over time.

Inbreeding avoidance influences the viability of reintroduced populations of African wild dogs (Lycaon pictus).

The conservation of many fragmented and small populations of endangered African wild dogs (Lycaon pictus) relies on understanding the natural processes affecting genetic diversity, demographics, and future viability. We used extensive behavioural, life-history, and genetic data from reintroduced African wild dogs in South Africa to (1) test for inbreeding avoidance via mate selection and (2) model the potential consequences of avoidance on population persistence. Results suggested that wild dogs avoided mating with kin. Inbreeding was rare in natal packs, after reproductive vacancies, and between sibling cohorts (observed on 0.8%, 12.5%, and 3.8% of occasions, respectively). Only one of the six (16.7%) breeding pairs confirmed as third-order (or closer) kin consisted of animals that were familiar with each other, while no other paired individuals had any prior association. Computer-simulated populations allowed to experience inbreeding had only a 1.6% probability of extinction within 100 years, whereas all populations avoiding incestuous matings became extinct due to the absence of unrelated mates. Populations that avoided mating with first-order relatives became extinct after 63 years compared with persistence of 37 and 19 years for those also prevented from second-order and third-order matings, respectively. Although stronger inbreeding avoidance maintains significantly more genetic variation, our results demonstrate the potentially severe demographic impacts of reduced numbers of suitable mates on the future viability of small, isolated wild dog populations. The rapid rate of population decline suggests that extinction may occur before inbreeding depression is observed.

Transmission of parental care behavior in African striped mice, Rhabdomys Pumilio

The expression of behavior, including parental care behavior, is influenced by complex interactions of the genes of an organism and the prevailing environmental conditions. Previously, we showed that the development of paternal, but not maternal, care in the African striped mouse, Rhabdomys pumilio, has a significant nongenetic maternal component. Here, we investigate the genetic component of parental care behavior from parents to offspring. We first measured the duration of parental care behavior of mothers and fathers every second day for 11 days postnatally. Subsequently, one son and one daughter from each of these litters were paired with unrelated mates when they were adults and their parental care behavior scored. Using regression models, we then compared parental care behavior of parents and their adult offspring. The transmission of parental care behavior from striped mouse fathers to sons and from mothers to both sons and daughters did not indicate a genetic component. Instead, we found a patrilineal genetic component for parental care in daughters. The reason for this unusual pattern of inheritance is not known, but this finding complements that of our other studies, showing that the expression of maternal care behavior in adult daughters is also not nongenetically influenced by their mothers. We suggest that, although females are constrained to provide maternal care in different social contexts, maternal care behavior may be influenced genetically by the father.

Cryptic female preference for genetically unrelated males is mediated by ovarian fluid in the guppy

As inbreeding is costly, it has been suggested that polyandry may evolve as a means to reduce the negative fitness consequences of mating with genetically related males. While several studies provide support for this hypothesis, evidence of pure post-copulatory mechanisms capable of biasing paternity towards genetically unrelated males is still lacking; yet these are necessary to support inbreeding avoidance models of polyandry evolution. Here we showed, by artificially inseminating a group of female guppies with an equal number of sperm from related (full-sib) and unrelated males, that sperm competition success of the former was 10 per cent lower, on average, than that of the unrelated male. The paternity bias towards unrelated males was not due to differential embryo survival, as the size of the brood produced by control females, which were artificially inseminated with the sperm of a single male, was not influenced by their relatedness with the male. Finally, we collected ovarian fluid (OF) from virgin females. Using computer-assisted sperm analysis, we found that sperm velocity, a predictor of sperm competition success in the guppy, was significantly lower when measured in a solution containing the OF from a sister as compared with that from an unrelated female. Our results suggest that sperm-OF interaction mediates sperm competition bias towards unrelated mates and highlight the role of post-copulatory mechanisms in reducing the cost of mating with relatives in polyandrous females.

Inbreeding depression in development, survival, and reproduction in the adzuki bean beetle (Callosobruchus chinensis)

AbstractInbreeding depression of an aspect of fitness is observed in many insects, but the traits that are of importance for inbreeding depression of fitness remain poorly understood. Here the magnitude of inbreeding depression of fitness‐related traits in the development and adult stages was measured in a captive population of the adzuki bean beetle, Callosobruchus chinensis (Coleoptera: Bruchidae). Beetles produced by full‐sib matings had 8% lower survival in the development stage than did beetles produced by unrelated matings. Although inbred and outbred offspring did not differ in body size after emergence, inbred offspring took 2–3% longer to develop to emergence. This indicates inbreeding depression of growth rate. At the adult stage, inbreeding had no significant effect on longevity, however lifetime offspring production was reduced by 11%. Thus, the magnitude of inbreeding depression was relatively large for offspring production. This suggests inbreeding depression of fitness manifests, to a particularly significant extent, in reduced productivity. This study shows the C. chinensis population, which has been in captivity for more than 100 generations, harbors genetic loads.

Social biology of rodents

Herein, I summarize some basic components of rodent social biology. The material in this paper is summarized and condensed from a recent book "Rodent Societies: An Ecological and Evolutionary Perspective" edited by J. O. Wolff and P. W. Sherman (2007). I describe the four basic spacing patterns and illustrate how female territoriality is a function of offspring defense and male mating tactics are a function of female defensibility. The vulnerability of young to infanticide shapes female spacing and mating behavior. Food does not appear to be a defensible resource for rodents, except for those species that larder hoard nonperishable items such as seeds. Philopatry and the formation of kin groups result in genetic sub-structuring of the population, which in turn affects effective population size and genetic diversity. Dispersal is male biased and typically involves emigration from the maternal site to avoid female relatives and to seek unrelated mates. Scent marking is a major form of communication and is used in reproductive competition and to assess prospective mates, but it is also eavesdropped by predators to locate prey. Females do not appear to alter the sex ratio of litters in response to maternal condition but among arvicoline rodents daughters appear to be favored in spring and sons in autumn. Rodents are relatively monomorphic; however, females tend to be larger than males in the smallest species and smaller in the larger species. Predation risk results from an interaction among foraging time and vulnerability and in turn affects behavioral and life history characteristics.

The causes of physiological suppression among female meerkats: A role for subordinate restraint due to the threat of infanticide?

In many animal societies, subordinates exhibit down-regulated reproductive endocrine axes relative to those of dominants, but whether this ‘physiological suppression’ arises from active interference by dominants or subordinate self-restraint is a matter of debate. Here we investigate the roles that these processes play in precipitating physiological suppression among subordinate female meerkats, Suricata suricatta. We show that, while subordinate females are known to suffer stress-related physiological suppression during periodic temporary evictions by the dominant female, their low estrogen levels while within their groups cannot be readily attributed to chronic stress, as their fecal glucocorticoid metabolite levels during this time are comparable to those of dominants. The low estrogen levels of subordinate females also cannot be explained simply by self-restraint due to factors that could reduce their payoff from maintaining their fertility regardless of the presence of the dominant female (young age, a lack of unrelated mates, poor body condition and limited breeding experience), as substantial rank-related differences in fecal total-estrogen metabolite levels remain when such factors are controlled. We suggest that this residual difference in estrogen levels may reflect a degree of subordinate restraint due in part to the dominant female's ability to kill their young. Accordingly, subordinate female estrogen levels vary in association with temporal variation in the likelihood of infanticide by the dominant. Attempts to identify the causes of physiological suppression should be cautious if rejecting any role for dominant interference in favor of subordinate restraint, as the dominant's capacity to interfere may often be the reason why subordinates exercise restraint.

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.

Molecular-genetic analyses of dispersal and breeding behaviour in the Australian termite Coptotermes lacteus: evidence for non-random mating in a swarm-dispersal mating system

We used microsatellite DNA markers to infer the dispersal and breeding behaviour of Coptotermes lacteus, a termite whose large mounds are a conspicuous feature of Australia’s central east coast. We genotyped a subsample of neuter offspring for each of 38 colonies sampled over two spatially separated populations, one in a natural forest and the other in an exotic radiata pine plantation. All colonies showed offspring genotype frequencies consistent with a single reproductive pair. This result confirms that stable monogamy is the normal breeding arrangement for this species and that multi-reproductive colonies are rare. The two study populations were significantly differentiated and the distance separating them (~150 km) is therefore an effective constraint on gene flow. The populations themselves, however, were not noticeably subdivided above the level of colony. This lack of within-population viscosity is unexpected for weakly dispersing species and suggests that local gamete dispersal is in fact quite effective in C. lacteus. Nonetheless, dispersing sexuals do not appear to mate randomly. Instead, all four microsatellite loci are deficient in heterozygotes, indicating that populations are substantially inbred, irrespective of habitat. Evidence from hierarchical F-statistics, spatial genetic autocorrelation and relatedness calculations suggests that deviations from Hardy–Weinberg equilibrium may result from either a preference for non-sibling relatives over totally unrelated mates, or from random mating with viscosity – though evidence for the latter hypothesis was not detected. These findings suggest that swarm-dispersal mating systems, usually considered to produce outbreeding and panmixia, can instead involve a notable degree of non-random mating.

Asymmetry in age suppresses reproduction in female woodland voles, Microtus pinetorum

The partitioning of reproduction in animal societies is a topic of interest to those studying animal behaviour. Under some conditions, two or more females may breed, but lack of reproduction by the younger females occurs frequently. Lack of reproduction by young females may be due to kin asymmetry, dominance asymmetry, or incest avoidance. We conducted breeding experiments to distinguish among these three hypotheses. We show that female reproduction within woodland vole family groups becomes skewed as the asymmetry in age, which is correlated with dominance, between females increases. When daughters were housed with their mothers and a potential mate and the age difference between females was large, we found a high level of skew as compared to females housed with same-age sisters and a potential mate or females housed only with a potential mate. We argue that dominance asymmetry is the best explanation for reproductive skew seen in female woodland voles that have access to unfamiliar, unrelated mates based on reproductive and previous behavioural observations.

The Effects of Inbreeding on Male Courtship Behaviour and Coloration in Guppies

AbstractDespite an extensive literature on inbreeding depression in a variety of traits, relatively little is known about the effects of inbreeding on patterns of sexual behaviour. In this study, we use the guppy Poecilia reticulata to investigate the influence of parental relatedness (full‐sib. vs. unrelated matings) on sexual behaviour and colour pattern variation in adult male offspring. Our results revealed that one generation of full‐sibling mating resulted in a strong decline in male sexual motivation (courtship intensity and following behaviour) and mating success (number of successful copulations and insemination success – as estimated by the frequency of post‐copulatory jerks after mating), but we detected no significant influence of inbreeding on colour pattern variation. Our finding that sexual ornamentation (colour) did not show similar inbreeding depression to courtship behaviour may be due to differences in the genetic basis of these traits. Our findings indicate that courtship can be a sensitive indicator of genetic stress and add to an emerging picture that sexually selected traits can be severely affected by inbreeding depression.

Adaptive genetic complementarity in mate choice coexists with selection for elaborate sexual traits

Choice of genetically unrelated mates is widely documented, yet it is not known how self-referential mate choice can co-occur with commonly observed directional selection on sexual displays. Across 10 breeding seasons in a wild bird population, we found strong fitness benefits of matings between genetically unrelated partners and show that self-referential choice of genetically unrelated mates alternates with sexual selection on elaborate plumage. Seasonal cycles of diminishing variation in ornamentation, caused by early pairing of the most elaborated males, and influx of increasingly genetically unrelated available mates caused by female-biased dispersal, lead to temporal fluctuations in the target of mate choice and enabled coexistence of directional selection for ornament elaboration with adaptive pairing of genetically unrelated partners.

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.

Great frigatebirds, Fregata minor, choose mates that are genetically similar

Inbreeding occurs infrequently in most natural populations, with the level of relatedness between mates potentially being influenced by behavioural mechanisms of mate choice and spatial genetic structure of the population. We studied mate relatedness in a Hawaiian population of great frigatebirds with the expectation, based on frigatebird ecology, that mated pairs were unlikely to be more genetically similar than a random draw of adults from the breeding population. We used a paired analysis to compare the DNA fingerprint similarity of a female and her mate versus the same female and a random male that was breeding elsewhere on the same island. Overall, band-sharing scores between mates were higher than band-sharing scores between nonmates, and the mean coefficient of relatedness between mates was 0.082. Relatedness between mates was not a consequence of strong natal philopatry coupled with random mate choice: historical data revealed several recent between-island shifts in the location of the breeding colony, and the degree of genetic similarity between nonmates was not well predicted by the physical distance between their nest sites on Tern Island. Instead, females may deliberately choose related individuals as mates. Tests for a relationship between the genetic similarity of mates and the size and ectoparasite load of their 1-week-old chick were equivocal. The question of how and why females may be choosing genetically similar mates is unresolved, but it appears to be a consequence of active choice rather than spatial genetic structure or limited availability of unrelated mates.

Mate choice in the predaceous mite Phytoseiulus persimilis: evidence of self‐referent phenotype matching?

AbstractClose inbreeding may have negative fitness effects. Consequently, organisms have evolved various mechanisms, which enable them to avoid close inbreeding. In no‐choice and choice experiments we assessed whether the predaceous mite Phytoseiulus persimilis Athias‐Henriot (Acari: Phytoseiidae) avoids close inbreeding by kin recognition. No‐choice experiments demonstrated that virgin females more readily accept unrelated males than they accept related ones, which suggests a female preference for unrelated mates. Because each female had been reared in isolation prior to experiments, females most likely imprinted on themselves, and later used self‐referent phenotype matching to assess potential mating partners. In contrast, neither female nor male choice experiments indicated a preference. Analyses of female and male behavior revealed that in choice experiments, female preference for unrelated males was probably confounded by male competition and/or altered by the different ecological context posed by choice experiments.

Absence of extra-pair fertilisations in the Chinstrap Penguin Pygoscelis antarctica

We analysed genetic relatedness through DNA-fingerprinting in 38 two-chick families of Chinstrap Penguins Pygoscelis antarctica in the Vapour Col colony on Deception Island, Antarctica. Band-sharing coefficients between males and chicks in their nests, females and chicks in their nests and brood mates were very close to 0.50 and were not significantly different. Presumably unrelated pair mates showed much lower band-sharing coefficients (0.12), which differed significantly from those between putative parents and their chicks and between presumed siblings. No case of extra-pair paternity was detected according to the presence of novel bands or to band-sharing coefficients. Monogamy in the study population is not only social but also genetic.