Genetic consequences of natal dispersal in the colonial lesser kestrel

Dispersal is a life-history trait that plays a fundamental role in population dynamics, influencing evolution, species distribution, and the genetics and structure of populations. In spite of the fact that dispersal has been hypothesized to be an efficient behavioural mechanism to avoid inbreeding, the expected relationship between dispersal and mate relatedness still remains controversial. Here, we examine the genetic consequences of natal dispersal, namely the higher chance of obtaining genetically less similar mates as a result of moving from natal to breeding sites, in a lesser kestrel (Falco naumanni) population. Relatedness between individuals tended to decrease with distance between their breeding colonies, indicating that the study population follows an 'isolation-by-distance' pattern of spatial genetic structure. Such a fine-scale genetic structure generates a scenario in which individuals can potentially increase the chance of obtaining genetically less similar mates by dispersing over larger distances from their natal colony. Using dispersal information and genotypic data, we showed that mate relatedness decreased with natal dispersal distance, an effect that remained significant both while including and excluding philopatric individuals from the data set. These results, together with the well known detrimental consequences of reduced genetic diversity in the study population, suggest that dispersal may have evolved, at least in part, to avoid the negative fitness consequences of mating with genetically similar individuals.     

Prevalence of multiple mating by female common dormice, <Emphasis Type="Italic">Muscardinus avellanarius</Emphasis>

Mating behaviour is an important component of species’ life histories. Knowledge of natural patterns of mating can lead also to more effective management strategies for populations of conservation concern. Despite a high conservation profile many aspects of the biology of the common dormouse (Muscardinus avellanarius) remain unknown, potentially limiting present conservation efforts. We determine the mating behaviour of M. avellanarius at two woodland sites in the UK: (1) Bontuchel (a natural population in Wales) and (2) Wych (a population in England that was established by reintroducing captive-bred animals) by genotyping mothers and litters at a panel of 10 microsatellite loci. Adult female body weight positively correlates with litter size and no apparent reproductive skew was evident. We found that multiple mating by female dormice is prevalent at both sites, with litters containing three or more offspring sired by multiple fathers; moreover, multiple mating is adopted by released animals even after a period of captive breeding where females are mated singly or as a breeding pair. We also present evidence for low proportion of fathers identified in our samples that probably related to unsampled individuals and/or larger than anticipated population sizes. This first report of mating behaviour in M. avellanarius highlights the role of genetic studies to uncover species’ reproductive behaviours and include these data for conservation management.     

Multiple paternity in wild populations of invasive

Multiple paternity within litters has been recorded among a variety of small mammal species, including some species of rodents. Although multiple mating has been observed in wild Rattus populations, whether such mating results in litters with multiple paternities has not been established previously. For studies involving invasive species, awareness is useful of the level of genetic diversity a single pregnant invader can bring to a population. Multiple paternity is a means of providing additional genetic diversity to founding populations of rats on islands, which might improve population fitness. We used a genetic approach to confirm that multiple paternity occurs in wild populations of two rat species (Rattus norvegicus and R. rattus) in New?Zealand. This was accomplished by genotyping litters of embryos in pregnant females, and subtracting the known maternal alleles to find the number of paternal alleles necessary to form the litter. The number of paternal contributors cannot be overestimated by this method, befitting a conservative approach to the detection of multiple paternity, but can be underestimated. We used simulations to investigate the level of underestimation likely under two possible scenarios involving multiple paternity.     

Punishment of polygyny

We investigated the evolution of monogamy (one male, one female) and polygyny (one male, more than one female). In particular, we studied whether it is possible for a mutant polygynous mating strategy to invade a resident population of monogamous breeders and, alternatively, whether a mutant monogamy can invade resident polygyny. Our population obeys discrete-time Ricker dynamics. The role of males and females in the breeding system is incorporated via the harmonic birth function. The results of the invasability analysis are straightforward. Polygyny is an evolutionarily stable strategy mating system; this holds throughout the examined range of numbers of offspring produced per female. So that the two strategies can coexist, polygyny has to be punished. The coexistence of monogamy and polygyny is achieved by reducing the offspring number for polygyny relative to monogamy. This yields long-term persistence of the strategies for all offspring numbers studied. An alternative punishment is to increase the sensitivity of polygynous breeders to population density. The coexistence is possible only with a limited range of offspring produced. The third way to achieve coexistence of the two mating strategies is to assume that individuals live in a spatially structured population, where dispersal links population subunits to a network. Reducing the dispersal rate of polygynous breeders relative to that of monogamous individuals makes the coexistence feasible. However, for monogamy to persist, the number of offspring produced has to be relatively high.     

Males and Females Contribute Unequally to Offspring Genetic Diversity in the Polygynandrous Mating System of Wild Boar

The maintenance of genetic diversity across generations depends on both the number of reproducing males and females. Variance in reproductive success, multiple paternity and litter size can all affect the relative contributions of male and female parents to genetic variation of progeny. The mating system of the wild boar (Sus scrofa) has been described as polygynous, although evidence of multiple paternity in litters has been found. Using 14 microsatellite markers, we evaluated the contribution of males and females to genetic variation in the next generation in independent wild boar populations from the Iberian Peninsula and Hungary. Genetic contributions of males and females were obtained by distinguishing the paternal and maternal genetic component inherited by the progeny. We found that the paternally inherited genetic component of progeny was more diverse than the maternally inherited component. Simulations showed that this finding might be due to a sampling bias. However, after controlling for the bias by fitting both the genetic diversity in the adult population and the number of reproductive individuals in the models, paternally inherited genotypes remained more diverse than those inherited maternally. Our results suggest new insights into how promiscuous mating systems can help maintain genetic variation.     

Spatial genetic structure in continuous and fragmented populations of Pinus pinaster Aiton

Habitat fragmentation, i.e., the reduction of populations into small isolated remnants, is expected to increase spatial genetic structure (SGS) in plant populations through nonrandom mating, lower population densities and potential aggregation of reproductive individuals. We investigated the effects of population size reduction and genetic isolation on SGS in maritime pine ( Pinus pinaster Aiton) using a combined experimental and simulation approach. Maritime pine is a wind-pollinated conifer which has a scattered distribution in the Iberian Peninsula as a result of forest fires and habitat fragmentation. Five highly polymorphic nuclear microsatellites were genotyped in a total of 394 individuals from two population pairs from the Iberian Peninsula, formed by one continuous and one fragmented population each. In agreement with predictions, SGS was significant and stronger in fragments ( Sp  = 0.020 and Sp  = 0.026) than in continuous populations, where significant SGS was detected for one population only ( Sp  = 0.010). Simulations suggested that under fat-tailed dispersal, small population size is a stronger determinant of SGS than genetic isolation, while under normal dispersal, genetic isolation has a stronger effect. SGS was always stronger in real populations than in simulations, except if unrealistically narrow dispersal and/or high variance of reproductive success were modelled (even when accounting for potential overestimation of SGS in real populations as a result of short-distance sampling). This suggests that factors such as nonrandom mating or selection not considered in the simulations were additionally operating on SGS in Iberian maritime pine populations.     

The effect of habitat fragmentation on dispersal patterns, mating behavior, and genetic variation in a pika (Ochotona princeps) metapopulation

 Habitat fragmentation is becoming increasingly common, yet, the effect of habitat spatial structure on population dynamics remains undetermined for most species. Populations of a single species found in fragmented and nonfragmented habitat present a rare opportunity to examine the effect of habitat spatial structure on population dynamics. This study investigates the impact of highly fragmented habitat on dispersal patterns, mating behavior, and genetic variation in a pika (Ochotona princeps) population with a mainland-island spatial structure. Juvenile dispersal patterns in fragmented habitat revealed that individuals tended to disperse to neighboring habitat patches. However, within-patch band-sharing scores from multilocus DNA fingerprints did not differ from what would be expected if individuals were assorting randomly among habitat patches each year. Multiple, short-distance dispersal targets for juveniles and occasional long-distance dispersal events suggest that habitat fragmentation on this scale has not resulted in restricted dispersal and a genetically subdivided population. Although pikas tended to mate with the closest available partner, DNA fingerprinting band-sharing scores between mated pairs were consistent with a random mating hypothesis. Random mating in this population appears to be an incidental effect of dispersal in a fragmented habitat. This pattern is distinct from that found in nonfragmented habitat (large talus patches) where mating was non-random and consistent with mating between individuals of intermediate relatedness. DNA fingerprinting data revealed within-species variation in the mating habits of the pika directly attributable to habitat spatial structure. Received: 4 November 1996 / Accepted: 30 June 1997     

Cryptic behaviours, inverse genetic landscapes, and spatial avoidance of inbreeding in the Pacific jumping mouse

Although the behaviour of individuals is known to impact the genetic make-up of a population, observed behavioural patterns do not always correspond to patterns of genetic structure. In particular, philopatric or dispersal-limited species often display lower-than-expected values of relatedness or inbreeding suggestive of the presence of cryptic migration, dispersal, or mating behaviours. I used a combination of microsatellite and mark-recapture data to test for the influence of such behaviours in a dispersal-limited species, the Pacific jumping mouse, within a semi-isolated population over three seasons. Despite short dispersal distances and a low rate of first generation migrants, heterozygosities were high and inbreeding values were low. Dispersal was male-biased; interestingly however, this pattern was only present when dispersal was considered to include movement away from paternal home range. Not unexpectedly, males were polygynous; notably, some females were also found to be polyandrous, selecting multiple neighbouring mates for their single annual litter. Patterns of genetic structure were consistent with these more inconspicuous behavioural patterns. Females were more closely related than males and isolation by distance was present only in females. Furthermore, detailed genetic landscapes revealed the existence of strong, significant negative correlations, with areas of low genetic distance among females overlapping spatially with areas of high genetic distance among males. These results support the hypothesis that the detected cryptic components of dispersal and mating behaviour are reducing the likelihood of inbreeding in this population through paternally driven spatial mixing of male genotypes and polyandry of females.     

The first reproductive parameters and evidence of multiple paternity in one new spiny dogfish species,Squalus albicaudus (Squaliformes,Squalidae)

Understanding elasmobranch reproductive biology is necessary for species conservation. Multiple paternity (MP) has been reported for elasmobranchs, and this study investigates the reproductive aspects and mating system (paternity genetic analyses) for Squalus albicaudus. Thirteen pregnant females were analysed concerning reproductive parameters, and the mating system was assessed for nine females and their litters. The study found a mean fecundity of 2.84 pups per litter without correlation between total female length and the number of embryos per litter. One litter showed evidence of MP, indicating the presence of polyandrous behaviour of the species.     

Social Mating System and Sex-Biased Dispersal in Mammals and Birds: A Phylogenetic Analysis

The hypothesis that patterns of sex-biased dispersal are related to social mating system in mammals and birds has gained widespread acceptance over the past 30 years. However, two major complications have obscured the relationship between these two behaviors: 1) dispersal frequency and dispersal distance, which measure different aspects of the dispersal process, have often been confounded, and 2) the relationship between mating system and sex-biased dispersal in these vertebrate groups has not been examined using modern phylogenetic comparative methods. Here, we present a phylogenetic analysis of the relationship between mating system and sex-biased dispersal in mammals and birds. Results indicate that the evolution of female-biased dispersal in mammals may be more likely on monogamous branches of the phylogeny, and that females may disperse farther than males in socially monogamous mammalian species. However, we found no support for a relationship between social mating system and sex-biased dispersal in birds when the effects of phylogeny are taken into consideration. We caution that although there are larger-scale behavioral differences in mating system and sex-biased dispersal between mammals and birds, mating system and sex-biased dispersal are far from perfectly associated within these taxa.     

Proximity-dependent pollen performance in Silene vulgaris

BACKGROUND AND AIMS: Pollen and seed dispersal in herbaceous insect-pollinated plants are often restricted, inducing strong population structure. To what extent this influences mating within and among patches is poorly understood. This study investigates the influence of population structure on pollen performance using controlled pollinations and genetic markers. METHODS: Population structure was investigated in a patchily distributed population of gynodioecious Silene vulgaris in Switzerland using polymorphic microsatellite markers. Experimental pollinations were performed on 21 hermaphrodite recipients using pollen donors at three spatial scales: (a) self-pollination; (b) within-patch cross-pollinations; and (c) between-patch cross-pollinations. Pollen performance was then compared with respect to crossing distance. KEY RESULTS: The population of S. vulgaris was characterized by a high degree of genetic sub-structure, with neighbouring plants more related to one another than to distant individuals. Inbreeding probably results from both selfing and biparental inbreeding. Pollen performance increased with distance between mates. Between-patch pollen performed significantly better than both self- and within-patch pollen donors. However, no significant difference was detected between self- and within-patch pollen donors. CONCLUSIONS: The results suggest that population structure in animal-pollinated plants is likely to influence mating patterns by favouring cross-pollinations between unrelated plants. However, the extent to which this mechanism could be effective as a pre-zygotic barrier preventing inbred mating depends on the patterns of pollinator foraging and their influence on pollen dispersal.     

Social organization of the voleClethrionomys rufocanus and its demographic and genetic consequences: A review

Recent findings on the relationship between social interaction and demographic process in the gray-sided voleClethrionomys rufocanus are reviewed with reference to the findings in other microtine rodents. Social behavior was particularly focused on spacing and dispersal, and their effects on population dynamics are discussed. Female territoriality can limit a population abundance as a density-dependent factor, although its regulatory effect is controversial. Female philopatry and male-biased dispersal should bring about the clumped distribution of female relatives and genetically random distribution of males during the breeding season. The sexual difference in dispersal patterns can contribute to the mating behavior of the vole; promiscuous mating and low frequency of incestuous mating. However, effects of social structure, including kinship, on reproduction and survival of individuals still remains to be clarified. Molecular markers may help to solve these issues and provide new field of population ecology in microtine rodents.     

Mating patterns and pollen dispersal in a heterodichogamous tree, Juglans mandshurica (Juglandaceae)

Mating patterns in heterodichogamous species are generally considered to be disassortative between flowering morphs, but this hypothesis has hitherto not been vigorously tested. Here, mating patterns and pollen dispersal were studied in Juglans mandshurica, a heterodichogamous wind-pollinated species that is widely distributed in northern and north-eastern China. Paternity analyses carried out on 11 microsatellite loci were used to estimate morph-specific rates of outcrossing and disassortative mating. Pollen dispersal and genetic structure were also investigated in the population under study. The mating pattern of J. mandshurica was highly outcrossing and disassortative. Pairwise values of intramorph relatedness were much higher than those of intermorph relatedness, and a low level of biparental inbreeding was detected. There was no significant difference in outcrossing and disassortative mating rates between the two morphs. The effective pollen dispersal distribution showed an excess of near-neighbor matings, and most offspring of individual trees were sired by one or two nearby trees. These results corroborate the previous suggestion that mating in heterodichogamous plant species is mainly disassortative between morphs, which not only prevents selfing but also effectively reduces intramorph inbreeding.     

Comparison of life-history characteristics of island and mainland populations of the swamp antechinus

The reproductive ecology of the swamp antechinus Antechinus minimus , a small dasyurid (Dasyuridae) marsupial with obligate male semelparity, was investigated in populations inhabiting the mainland coast and on a nearby offshore island in south-eastern Australia. The size and sex ratios of litters, individual body mass and size, timing of births and female longevity were determined from live-trapped animals. The island population had significantly smaller litter sizes and greater adult body mass in comparison with the mainland population. This is consistent with features of the 'island syndrome', which predicts directional selection for these traits in high-density populations with reduced extrinsic mortality. However, inter-annual variability in litter sizes in the island population suggests that litter size is more responsive to fluctuating local conditions, such as population density, which is likely to affect food availability, rather than directional genetic changes. In contrast with other antechinus species, biased sex ratios were not evident. In addition, large variations of the timing of births were estimated at both sites and these appear to be related to seasonal conditions such as autumn rainfall and female body mass before mating.     

Within‐population variation in social strategies characterize the social and mating system of an Australian lizard,Egernia whitii

The lizard genus Egernia has been suggested as an excellent model system for examining the evolution of sociality as it exhibits considerable diversity in social organization both between and within species. To date the majority of work examining the factors responsible for the evolution of sociality within Egernia has advocated a broad scale approach; identifying the social structure of specific species or populations and comparing the degree of sociality between them. However, we argue that significant advancements could also be gained by examining variation in social strategies within populations. Here we integrate a detailed, 3‐year, field‐based examination of social spacing and juvenile dispersal with molecular analyses of paternity to determine the social and mating system of a Tasmanian population of White's skink (Egernia whitii). We show that E. whitii live in small stable family groups consisting of an adult male, his female partner(s), as well as juvenile or sub‐adults individuals. In addition, while the mating system is characterized by considerable genetic monogamy, extra‐pair fertilizations are relatively common, with 34% of litters containing offspring sired by males from outside the social group. We also show that traits related to social organization (social group composition, group size, stability and the level of extra‐pair paternity) vary both between and within individuals. We suggest that ecological factors, such as habitat saturation, quality and availability, play a key role in maintaining between individual variation in social strategies, and that examining these individual level processes will allow us to more clearly understand variation in sociality among species.     

Genetic assessment of paternity and relatedness in a managed population of cougars

Understanding the social dynamics of large carnivores is critical to effective conservation and management planning. We made the first attempt to delineate both paternity and relatedness for a population of cougar (Puma concolor) using microsatellite data. We analyzed a long-term genetic dataset collected from a hunted population in the Garnet Mountains of western Montana. We assigned paternity for 62.5% of litters sampled using both exclusion and likelihood analyses. Attempts at reconstructing unsampled paternal genotypes resulted in delineating possible sires for 8 more litters. Sires were on average younger than reported for males involved in pairings assessed via field data in other cougar populations. Although most mating pairs were unrelated, 5 of 17 pairings involved cougars with levels of relatedness corresponding to half-sibling and full-sibling or parent offspring relationship (r = 0.215–0.575). Relatedness among adult and subadult males was higher than relatedness levels among adult and subadult females. Relatedness among males in the Garnet population differed from patterns hypothesized to occur under male-biased dispersal theories for cougars. The long-term impact of the turnover of resident cougars in hunted populations is still unclear and warrants additional research. Our results highlight the utility of monitoring cougar demographic parameters using a combination of genetic and field data that in turn may assist managers with determining cougar harvest quotas or strategies, harvest seasons, sustainable harvest, and the appropriate management level of cougar populations. © 2011 The Wildlife Society.     

Inbreeding Avoidance Drives Consistent Variation of Fine-Scale Genetic Structure Caused by Dispersal in the Seasonal Mating System of Brandt’s Voles

Inbreeding depression is a major evolutionary and ecological force influencing population dynamics and the evolution of inbreeding-avoidance traits such as mating systems and dispersal. Mating systems and dispersal are fundamental determinants of population genetic structure. Resolving the relationships among genetic structure, seasonal breeding-related mating systems and dispersal will facilitate our understanding of the evolution of inbreeding avoidance. The goals of this study were as follows: (i) to determine whether females actively avoided mating with relatives in a group-living rodent species, Brandt’s voles (Lasiopodomys brandtii), by combined analysis of their mating system, dispersal and genetic structure; and (ii) to analyze the relationships among the variation in fine-genetic structure, inbreeding avoidance, season-dependent mating strategies and individual dispersal. Using both individual- and population-level analyses, we found that the majority of Brandt’s vole groups consisted of close relatives. However, both group-specific FISs, an inbreeding coefficient that expresses the expected percentage rate of homozygosity arising from a given breeding system, and relatedness of mates showed no sign of inbreeding. Using group pedigrees and paternity analysis, we show that the mating system of Brandt’s voles consists of a type of polygyny for males and extra-group polyandry for females, which may decrease inbreeding by increasing the frequency of mating among distantly-related individuals. The consistent variation in within-group relatedness, among-group relatedness and fine-scale genetic structures was mostly due to dispersal, which primarily occurred during the breeding season. Biologically relevant variation in the fine-scale genetic structure suggests that dispersal during the mating season may be a strategy to avoid inbreeding and drive the polygynous and extra-group polyandrous mating system of this species.     

Inbreeding is reduced by female-biased dispersal and mating behavior in Ethiopian wolves

Molecular tools have enabled wildlife researchers to obtainaccurate information on the kinship, mating behavior, and dispersalof individuals. We genotyped 192 Ethiopian wolves (n = 29 packs)in the Bale Mountains for 17 microsatellite loci to 1) elucidatekinship within and between packs, 2) assess parentage of pups,and 3) evaluate whether inbreeding is avoided by dispersal and/ormating behavior. Mean pairwise relatedness within packs (R =0.39) was significantly greater than that estimated from randomassignment of individuals to packs. However, breeding pairswere most often unrelated, suggesting that female-biased dispersalreduces inbreeding. We assigned maternity to 49 pups and paternityto 47 pups (n = 12 litters) using a combination of exclusion,likelihood analyses (using CERVUS software), and sibship reconstruction.Multiple paternity occurred in 33% of litters; extrapack paternityaccounted for 28% of all resolved paternities, occurring in50% of litters. We found no evidence that extrapack copulationsreduce inbreeding; however, more detailed analyses may elucidatethe effect of recent population declines and demographic disturbancesdue to recurring disease outbreaks. The adaptive advantagesof female-biased dispersal and the observed mating system arediscussed in relation to Ethiopian wolf sociobiology and ecology.     

High levels of genetic monogamy in the group-living Australian lizard Egernia stokesii

The Australian lizard Egernia stokesii lives in spatially and temporally stable groups of up to 17 individuals. We have recently shown that these groups are comprised of breeding partners, their offspring and, in some cases, highly related adults, providing the first genetic evidence of a family structure in any lizard species. Here we investigated the mating system of E. stokesii using data from up to eight polymorphic microsatellite loci and tested the hypothesis that breeding partners are monogamous both within and between mating seasons. Among 16 laboratory-born litters from field collected gravid females from two sites in South Australia, 75% had a single male parent and no male contributed to more than one litter, indicating a high level of genetic monogamy within a season. Additional analyses of field caught individuals, captured between 1994 and 1998, enabled assignment of parentage for 70 juveniles and subadults. These data showed that most young (88.6%) had both parents from within the same group and that high proportions of males (88.9%) and females (63.6%) have multiple cohorts of offspring only with the same partner. Our results suggest that monogamy both within and between seasons is a common mating strategy of E. stokesii and that breeding partners maintain stable associations together and with multiple cohorts of their offspring over periods of up to at least 5 years.     

Microevolution of S-allele frequencies in wild cherry populations: respective impacts of negative frequency dependent selection and genetic drift

Negative frequency dependent selection (NFDS) is supposed to be the main force controlling allele evolution at the gametophytic self-incompatibility locus (S-locus) in strictly outcrossing species. Genetic drift also influences S-allele evolution. In perennial sessile organisms, evolution of allelic frequencies over two generations is mainly shaped by individual fecundities and spatial processes. Using wild cherry populations between two successive generations, we tested whether S-alleles evolved following NFDS qualitative and quantitative predictions. We showed that allelic variation was negatively correlated with parental allelic frequency as expected under NFDS. However, NFDS predictions in finite population failed to predict more than half S-allele quantitative evolution. We developed a spatially explicit mating model that included the S-locus. We studied the effects of self-incompatibility and local drift within populations due to pollen dispersal in spatially distributed individuals, and variation in male fecundity on male mating success and allelic frequency evolution. Male mating success was negatively related to male allelic frequency as expected under NFDS. Spatial genetic structure combined with self-incompatibility resulted in higher effective pollen dispersal. Limited pollen dispersal in structured distributions of individuals and genotypes and unequal pollen production significantly contributed to S-allele frequency evolution by creating local drift effects strong enough to counteract the NFDS effect on some alleles.