Higher relatedness mitigates mortality in a nematode with lethal male fighting

According to kin selection theory, individuals show less aggression towards their relatives. Limited dispersal promotes interactions among relatives but also increases competition among them. The evolution of cooperation in viscous populations has been subject of mainly theoretical exploration. We investigated the influence of relatedness on aggression in males of entomopathogenic nematode Steinernema longicaudum that engage in lethal fighting. In a series of in vitro experiments, we found that both competitor male group size and relatedness influence male mortality rates. Higher relatedness led to progressively lower rates of male mortality. In experimentally infected insects, wherein large numbers of males and females interact, the proportion of dead and paralysed (= terminally injured) males was higher when infection was established by infective juveniles originating from a mixture of three lines than in those infected by a single line. The results collectively show that Steinernema longicaudum males recognize their kin and consequently male mortality rates are lower in groups consisting of more related males. Furthermore, this monotonic negative relationship between aggression and relatedness suggests that kin selection benefits are still substantial even under extreme competition. Our experiments also suggest that kin recognition in entomopathogenic nematodes has a genetic basis rather than being strictly based on environmental cues. We discuss our findings within the theoretical context of the evolution of altruistic/cooperative behaviour in structured populations.     

Pre-reproductive alliance formation in female wild house mice (<Emphasis Type="Italic">Mus domesticus</Emphasis>): the effects of familiarity and age disparity

Female house mice (Mus domesticus) are known to perform communal breeding more often with kin than with non-kin partners. When mice are grouped in semi-natural enclosures, related females develop pre-reproductive alliances more frequently than unrelated ones. However, little is known about the behavioural mechanisms and the factors promoting kin preferential cooperative associations in female mice. Here we evaluate the relative importance of familiarity and age disparity on the pre-reproductive development of agonistic behaviour and spatial associations within groups of three related females, freely interacting in semi-natural indoor enclosures. We found that familiarity clearly promoted female alliance formation by reducing aggression and enhancing spatial cohabitation, while genetic relatedness per se did not alleviate the effects of unfamiliarity on female grouping. Older sisters clearly dominated younger ones, even if they had lower body weights, or if they had to confront two allied littermate sisters. Hence, our findings corroborate previous findings on familiarity as a proxy for kin-preferential alliance formation in female mice. Moreover, we observed a strong impact of age stratification on female aggression-mediated dominance development. We suggest that this age effect could be expected from a queuing-for-reproduction view of younger house mouse females.Communicated by I. Schlupp     

Fine‐scale kin recognition in the absence of social familiarity in the Siberian jay,a monogamous bird species

Kin recognition is a critical element to kin cooperation, and in vertebrates, it is primarily based on associative learning. Recognition of socially unfamiliar kin occurs rarely, and it is reported only in vertebrate species where promiscuity prevents recognition of first‐order relatives. However, it is unknown whether the recognition of socially unfamiliar kin can evolve in monogamous species. Here, we investigate whether genetic relatedness modulates aggression among group members in Siberian jays (Perisoreus infaustus). This bird species is genetically and socially monogamous and lives in groups that are formed through the retention of offspring beyond independence, and the immigration of socially unfamiliar nonbreeders. Observations on feeders showed that genetic relatedness modulated aggression of breeders towards immigrants in a graded manner, in that they chased most intensely the immigrant group members that were genetically the least related. However, cross‐fostering experiments showed that breeders were equally tolerant towards their own and cross‐fostered young swapped as nestlings. Thus, breeders seem to use different mechanisms to recognize socially unfamiliar individuals and own offspring. As Siberian jays show a high degree of nepotism during foraging and predator encounters, inclusive fitness benefits may play a role for the evolution of fine‐scale kin recognition. More generally, our results suggest that fine‐graded kin recognition can evolve independently of social familiarity, highlighting the evolutionary importance of kin recognition for social species.     

Multiple paternity and kin recognition mechanisms in a guppy population

Help directed toward kin (nepotism) is an important example of social behaviour. Such helping behaviour requires a mechanism to distinguish kin from nonkin. The prevailing kin recognition hypothesis is that when familiarity is a reliable cue of relatedness, other mechanisms of recognition will not evolve. However, when familiarity is an unreliable cue of relatedness, kin recognition by phenotype matching is instead predicted to evolve. Here we use genetic markers to show that guppies (Poecilia reticulata) from a population in a tributary of the Paria River in Trinidad are characterized by a high degree of multiple mating with 95% of broods having more than one sire and some dams having offspring sired by six males. These levels of multiple mating are the highest reported among live-bearing fishes. The mean relatedness of brood-mates was 0.36 (as compared to 0.5 for full-siblings). Therefore, familiarity does not seem to be a reliable mechanism to assess full-sibling relatedness. Using two-choice behavioural trials, we found that juveniles from this population use both phenotype matching and familiarity to distinguish kin from nonkin. However, we did not find strong evidence that the guppies use these mechanisms to form shoals of related individuals as adults, which is similar to results from other guppy populations in Trinidad. The use of both familiarity and phenotype matching is discussed in the context of the Paria River guppy population's mating system and ecology. Overall, these data provide support for the kin recognition hypothesis and increase our understanding of the evolution of kin recognition systems.     

Genetic structure in the marbled rockfish (Sebastiscus marmoratus) across most of the distribution in the northwestern Pacific

The marbled rockfish (Sebastiscus marmoratus) is an important species that is widely distributed across the marginal seas of the northwestern Pacific. Several kinds of DNA markers, such as amplified fragment length polymorphisms (AFLP), mitochondrial DNA (mtDNA) and single nucleotide polymorphisms (SNPs), have been used to assess the population genetic characteristics of this species in previous studies. However, there have been no genetic profiling studies to cover the entire distribution. Here, six highly polymorphic microsatellite markers were applied to 18 populations across a spatially large area (from the Sea of Japan in the north to the South China Sea in the south). The results showed that the whole population exhibits high, stable genetic diversity, low relatedness and large effective population size. There was very weak genetic differentiation overall and no isolation by distance occurred among the populations, which may be attributed to significant contemporary gene flow, each generation. The above results may lead us to infer that the recent S. marmoratus population structure could be considered as one large integrated population. The present study will be beneficial to population conservation and fisheries management of S. marmoratus and will lead to better insights into the genetic characteristics of other species that belong to the Sebastidae family.     

Partitioning kin groups of broodstock in the critically endangered Chinese sturgeon,Acipenser sinensis Gray 1835

Pedigrees of broodstock with unknown relationship of the critically endangered Chinese sturgeon, Acipenser sinensis, was evaluated using microsatellite markers to facilitate genetic management in restocking programs with small broodstock size. We characterized the distributions of relatedness values to reconstruct kin groups in four hatchery families with known pedigrees using microsatellites. The distributions of relatedness values for kin classes were used for partitioning full sibling groups of wild A. sinensis broodstock kept in two hatcheries, resulted in 13 full sibling clusters, four of which containing 62% of all the wild individuals. This indicates high probability of choosing close related breeder pairs in random mating, thus selective breeding is necessary to minimize inbreeding and maintain genetic diversity. This study provides a useful tool for genetic management in conservation programs of A. sinensis in aim of preserving self‐sustained wild populations.     

Effects of Paternal Reproductive Tactic on Juvenile Behaviour and Kin Recognition in Chinook Salmon (Oncorhynchus tshawytscha)

Salmonids are characterized by alternative reproductive tactics, which can lead to an asymmetry in relatedness among offspring within nests and consequently the benefit of discriminating among nestmates. In this study, we examined the effect of paternal reproductive tactic on juvenile behaviour and kin discrimination in Chinook salmon. We created maternal half‐sibling families by collecting eggs from mature females and fertilizing one‐half with the milt of a precocious 2‐yr‐old male and the other half with the milt of a non‐precocious 4‐yr‐old male. These families were reared in full‐sibling groups for approximately 9 mo, and social interactions were then observed in groups of six fish of mixed relatedness. We found evidence for kin discrimination, as significantly less aggression was directed towards related fish than unrelated fish, and the same trends were observed regardless of whether social interactions included full‐siblings or half‐siblings. These results show that familiarity is not required to recognize kin and thereby implicate phenotype matching as the mechanism of kin recognition. We also found that the offspring of 2‐yr‐old males were larger and more aggressive than the offspring of 4‐yr‐old males, which is consistent with other studies showing that precocious males are the fastest‐growing members of their cohort. However, kin‐directed behaviours did not differ between the offspring of 2‐ and 4‐yr‐old males.     

Kin recognition and co‐operative foraging in Drosophila melanogaster larvae

A long‐standing goal for biologists and social scientists is to understand the factors that lead to the evolution and maintenance of co‐operative behaviour between conspecifics. To that end, the fruit fly, Drosophila melanogaster, is becoming an increasingly popular model species to study sociality; however, most of the research to date has focused on adult behaviours. In this study, we set out to examine group‐feeding behaviour by larvae and to determine whether the degree of relatedness between individuals mediates the expression co‐operation. In a series of assays, we manipulated the average degree of relatedness in groups of third‐instar larvae that were faced with resource scarcity, and measured the size, frequency and composition of feeding clusters, as well as the fitness benefits associated with co‐operation. Our results suggest that larval D. melanogaster are capable of kin recognition (something that has not been previously described in this species), as clusters were more numerous, larger and involved more larvae, when more closely related kin were present in the social environment. These findings are discussed in the context of the correlated fitness‐associated benefits of co‐operation, the potential mechanisms by which individuals may recognize kin, and how that kinship may play an important role in facilitating the manifestation of this co‐operative behaviour.     

No evidence that relatedness or familiarity modulates male harm in Drosophila melanogaster flies from a wild population

Sexual selection frequently promotes the evolution of aggressive behaviors that help males compete against their rivals, but which may harm females and hamper their fitness. Kin selection theory predicts that optimal male–male competition levels can be reduced when competitors are more genetically related to each other than to the population average, contributing to resolve this sexual conflict. Work in Drosophila melanogaster has spearheaded empirical tests of this idea, but studies so far have been conducted in laboratory‐adapted populations in homogeneous rearing environments that may hamper kin recognition, and used highly skewed sex ratios that may fail to reflect average natural conditions. Here, we performed a fully factorial design with the aim of exploring how rearing environment (i.e., familiarity) and relatedness affect male–male aggression, male harassment, and overall male harm levels in flies from a wild population of Drosophila melanogaster, under more natural conditions. Namely, we (a) manipulated relatedness and familiarity so that larvae reared apart were raised in different environments, as is common in the wild, and (b) studied the effects of relatedness and familiarity under average levels of male–male competition in the field. We show that, contrary to previous findings, groups of unrelated‐unfamiliar males were as likely to fight with each other and harass females than related‐familiar males and that overall levels of male harm to females were similar across treatments. Our results suggest that the role of kin selection in modulating sexual conflict is yet unclear in Drosophila melanogaster, and call for further studies that focus on natural populations and realistic socio‐sexual and ecological environments.     

Developmental aspects of kin recognition

The ability to recognise kin requires the individual to possess a variety of abilities. Individuals must produce a cue which indicates relatedness, they must process this cue to determine relatedness and then must act on this cue. Research has concentrated on the first and final stage of this process, i.e., the cues of kinship and kin correlated behaviour. Little attention has been paid to how individuals process cues to determine relatedness. This paper discusses how individuals ‘recognise’ kin, the exhibition of kin correlated behaviour and considers the role of the MHC in these processes. Two broad theories have emerged to explain how individuals recognise their kin: either a recognition gene(s) or some experiential mechanism. In mammals there is no evidence to suggest that recognition (the processing of the cue) is under genetic control but rather is the result of experience, learning about related individuals during development. Moreover studies on kin recognition in the domestic dog suggest that all kin are not recognised by the same process but different classes of kin, parents, siblings may well be recognised using different means. Studies of kin correlated behaviour suggest that the behaviour exhibited towards kin by Mongolian gerbils is mediated by the environment. Factors of environmental familiarity, sex and developmental age all affect the response of individuals to kin and non‐kin. In these situations the ability to recognise kin does not change but the exhibition of kin correlated behaviour changes according to environmental conditions. These studies indicate that kin recognition may not be the ‘unified’ process previously thought and thus any explanations of the proximate and ultimate causation of kin recognition need to encompass this complexity. The question remains of whether the MHC is complex enough to do so. This revised version was published online in July 2006 with corrections to the Cover Date.     

Genetic relatedness in wintering groups of house sparrows (Passer domesticus)

Social behaviour of group-living animals is often influenced by the relatedness of individuals, thus understanding the genetic structure of groups is important for the interpretation of costs and benefits of social interactions. In this study, we investigated genetic relatedness in feeding aggregations of free-living house sparrows ( Passer domesticus ) during the nonbreeding season. This species is a frequent model system for studies of social behaviour (e.g. aggression, social foraging), but we lack adequate information on the kin structure of sparrow flocks. During two winters, we ringed and observed sparrows at feeding stations, and used resightings to identify stable flock-members and to calculate association indices between birds. We genotyped the birds using seven highly polymorphic microsatellite loci, and estimated pairwise relatedness coefficients and relatedness categories (close kin vs. unrelated) by maximum likelihood method. We found that most birds were unrelated to each other in the flocks (mean ± SE relatedness coefficient: 0.06 ± 0.002), although most individuals had at least a few close relatives in their home flock (14.3 ± 0.6% of flock-mates). Pairwise association between individuals was not significantly related to their genetic relatedness. Furthermore, there was no difference between within-flock vs. between-flock relatedness, and birds had similar proportions of close kin within and outside their home flock. Finally, relatedness among members of different flocks was unrelated to the distance between their flocks. Thus, sparrow flocks were not characterized by association of relatives, nevertheless the presence of some close kin may provide opportunity for kin-biased behaviours to evolve.     

Kin Discrimination in a Macropod Marsupial

Differential treatment of kin is ubiquitous in social animals. Parents often behave preferentially towards their dependent offspring. Species in several taxa also bias behaviour towards non-descendent kin. This latter phenomenon has not been demonstrated in marsupials, which are reportedly less social than eutherian mammals. We report the first evidence of non-parental kin-biased behaviour in a macropodid marsupial. Experimental pairing of individuals based on kinship reliably altered the rate of aggression between individuals in pairs of female tammar wallabies ( Macropus eugenii ). This effect is probably attributable to relatedness rather than to familiarity. Marsupial sociality may be substantially more complex than is currently recognized.     

Kin and familiarity influence association preferences and aggression in the mangrove killifish Kryptolebias marmoratus

Association preferences and aggression intensity were investigated in relation to kin and familiarity in the self-fertilizing, clonal vertebrate, the mangrove killifish Kryptolebias marmoratus. Results indicated that fish preferentially associated with and exhibited less intense aggression towards members of their own genotype (kin), compared to members of a different genotype (non-kin). Furthermore, when fish were presented with stimulus groups of the same genotype that were familiar or unfamiliar, fish preferentially associated with and exhibited lower aggression intensity directed towards familiar groups. These results indicate that this species prefer to associate with both kin and familiar individuals and modulate aggression accordingly. These results are discussed with reference to the adaptive benefits of kin recognition and preferences for familiars, and place results within the context of current knowledge of the ecology of K. marmoratus.     

Does harvest affect genetic diversity in grey wolves?

Harvest can affect vital rates such as reproduction and survival, but also genetic measures of individual and population health. Grey wolves (Canis lupus) live and breed in groups, and effective population size is a small fraction of total abundance. As a result, genetic diversity of wolves may be particularly sensitive to harvest. We evaluated how harvest affected genetic diversity and relatedness in wolves. We hypothesized that harvest would (a) reduce relatedness of individuals within groups in a subpopulation but increase relatedness of individuals between groups due to increased local immigration, (b) increase individual heterozygosity and average allelic richness across groups in subpopulations and (c) add new alleles to a subpopulation and decrease the number of private alleles in subpopulations due to an increase in breeding opportunities for unrelated individuals. We found harvest had no effect on observed heterozygosity of individuals or allelic richness at loci within subpopulations but was associated with a small, biologically insignificant effect on within‐group relatedness values in grey wolves. Harvest was, however, positively associated with increased relatedness of individuals between groups and a net gain (+16) of alleles into groups in subpopulations monitored since harvest began, although the number of private alleles in subpopulations overall declined. Harvest likely created opportunities for wolves to immigrate into nearby groups and breed, thereby making groups in subpopulations more related over time. Harvest appears to affect genetic diversity in wolves at the group and population levels, but its effects are less apparent at the individual level given the population sizes we studied.     

Kinship reinforces cooperative predator inspection in a cichlid fish

Kin selection theory predicts that cooperation is facilitated between genetic relatives, as by cooperating with kin an individual might increase its inclusive fitness. Although numerous theoretical papers support Hamilton's inclusive fitness theory, experimental evidence is still underrepresented, in particular in noncooperative breeders. Cooperative predator inspection is one of the most intriguing antipredator strategies, as it implies high costs on inspectors. During an inspection event, one or more individuals leave the safety of a group and approach a potential predator to gather information about the current predation risk. We investigated the effect of genetic relatedness on cooperative predator inspection in juveniles of the cichlid fish Pelvicachromis taeniatus, a species in which juveniles live in shoals under natural conditions. We show that relatedness significantly influenced predator inspection behaviour with kin dyads being significantly more cooperative. Thus, our results indicate a higher disposition for cooperative antipredator behaviour among kin as predicted by kin selection theory.     

Short‐term variations in gene flow related to cyclic density fluctuations in the common vole

In highly fluctuating populations with complex social systems, genetic patterns are likely to vary in space and time due to demographic and behavioural processes. Cyclic rodents are extreme examples of demographically instable populations that often exhibit strong social organization. In such populations, kin structure and spacing behaviour may vary with density fluctuations and impact both the composition and spatial structure of genetic diversity. In this study, we analysed the multiannual genetic structure of a cyclic rodent, Microtus arvalis, using a sample of 875 individuals trapped over three complete cycles (from 1999 to 2007) and genotyped at 10 microsatellite loci. We tested the predictions that genetic diversity and gene flow intensity vary with density fluctuations. We found evidences for both spatial scale‐dependant variations in genetic diversity and higher gene flow during high density. Moreover, investigation of sex‐specific relatedness patterns revealed that, although dispersal is biased toward males in this species, distances moved by both sexes were lengthened during high density. Altogether, these results suggest that an increase in migration with density allows to restore the local loss of genetic diversity occurring during low density. We then postulate that this change in migration results from local competition, which enhances female colonization of empty spaces and male dispersal among colonies.     

Agricultural intensification alters marbled newt genetic diversity and gene flow through density and dispersal reduction

Recent agricultural intensification threatens global biodiversity with amphibians being one of the most impacted groups. Because of their biphasic life cycle, amphibians are particularly vulnerable to habitat loss and fragmentation that often result in small, isolated populations and loss of genetic diversity. Here, we studied how landscape heterogeneity affects genetic diversity, gene flow and demographic parameters in the marbled newt, Triturus marmoratus, over a hedgerow network landscape in Western France. While the northern part of the study area consists of preserved hedged farmland, the southern part was more profoundly converted for intensive arable crops production after WWII. Based on 67 sampled ponds and 10 microsatellite loci, we characterized regional population genetic structure and evaluated the correlation between landscape variables and (i) local genetic diversity using mixed models and (ii) genetic distance using multiple regression methods and commonality analysis. We identified a single genetic population characterized by a spatially heterogeneous isolation-by-distance pattern. Pond density in the surrounding landscape positively affected local genetic diversity while arable crop land cover negatively affected gene flow and connectivity. We used demographic inferences to quantitatively assess differences in effective population density and dispersal between the contrasted landscapes characterizing the northern and southern parts of the study area. Altogether, results suggest recent land conversion affected T. marmoratus through reduction in both effective population density and dispersal due to habitat loss and reduced connectivity.     

Host genetic determinants of the gut microbiota of wild mice

Identifying a common set of genes that mediate host–microbial interactions across populations and species of mammals has broad relevance for human health and animal biology. However, the genetic basis of the gut microbial composition in natural populations remains largely unknown outside of humans. Here, we used wild house mouse populations as a model system to ask three major questions: (a) Does host genetic relatedness explain interindividual variation in gut microbial composition? (b) Do population differences in the microbiota persist in a common environment? (c) What are the host genes associated with microbial richness and the relative abundance of bacterial genera? We found that host genetic distance is a strong predictor of the gut microbial composition as characterized by 16S amplicon sequencing. Using a common garden approach, we then identified differences in microbial composition between populations that persisted in a shared laboratory environment. Finally, we used exome sequencing to associate host genetic variants with microbial diversity and relative abundance of microbial taxa in wild mice. We identified 20 genes that were associated with microbial diversity or abundance including a macrophage‐derived cytokine (IL12a) that contained three nonsynonymous mutations. Surprisingly, we found a significant overrepresentation of candidate genes that were previously associated with microbial measurements in humans. The homologous genes that overlapped between wild mice and humans included genes that have been associated with traits related to host immunity and obesity in humans. Gene–bacteria associations identified in both humans and wild mice suggest some commonality to the host genetic determinants of gut microbial composition across mammals.     

Population Genetics,Dispersal, and Kinship Among Wild Squirrel Monkeys (Saimiri sciureus macrodon): Preferential Association Between Closely Related Females and Its Implications for Insect Prey Capture Success

Little genetic information is available to evaluate hypotheses concerning the parameters that affect population genetic structure in primate taxa that exhibit interspecific variation in social systems, such as squirrel monkeys (Saimiri). Here, we used genetic data to assess dispersal patterns, kin structure, and preferential association with same-sex kin in a wild population of Saimiri sciureus macrodon. We also analyzed behavioral data to assess whether individuals that maintain shorter interindividual distances show increased insect foraging success. If there was greater male than female dispersal, then we expected mean pairwise relatedness, F _ST values, and intragroup mean corrected assignment indices to be greater among adult females than among adult males. We also expected matrices of pairwise affinity indices (PAIs) for “association” (time spent ≤5 m) and “proximity” (time spent ≤10 m) among female dyads to positively correlate with a matrix of female pairwise relatedness. Not only did we find support for female philopatry, but we also found significant positive relationships between the relatedness matrix and each of the PAI matrices: females were more likely to be associated with (and proximal to) close female relatives than more distant relatives or unrelated individuals. Foraging analyses revealed that females had higher insect capture rates than males, and this sex difference may be related to a smaller mean interindividual distance among closely related female group members. Our result shows how estimates of genetic relatedness are useful for testing predictions regarding the evolution of sex-biased dispersal patterns, as well as potential relationships between kin-biased social behaviors and foraging success.     

How many came home? Evaluating ex situ conservation of green turtles in the Cayman Islands

Ex situ management is an important conservation tool that allows the preservation of biological diversity outside natural habitats while supporting survival in the wild. Captive breeding followed by re‐introduction is a possible approach for endangered species conservation and preservation of genetic variability. The Cayman Turtle Centre Ltd was established in 1968 to market green turtle (Chelonia mydas) meat and other products and replenish wild populations, thought to be locally extirpated, through captive breeding. We evaluated the effects of this re‐introduction programmme using molecular markers (13 microsatellites, 800‐bp D‐loop and simple tandem repeat mitochondrial DNA sequences) from captive breeders (N = 257) and wild nesting females (N = 57) (sampling period: 2013–2015). We divided the captive breeders into three groups: founders (from the original stock), and then two subdivisions of F₁ individuals corresponding to two different management strategies, cohort 1995 (“C1995”) and multicohort F₁ (“MCF1”). Loss of genetic variability and increased relatedness was observed in the captive stock over time. We found no significant differences in diversity among captive and wild groups, and similar or higher levels of haplotype variability when compared to other natural populations. Using parentage and sibship assignment, we determined that 90% of the wild individuals were related to the captive stock. Our results suggest a strong impact of the re‐introduction programmme on the present recovery of the wild green turtle population nesting in the Cayman Islands. Moreover, genetic relatedness analyses of captive populations are necessary to improve future management actions to maintain genetic diversity in the long term and avoid inbreeding depression.