Reproductive success and effective population size in woodrats (Neotoma macrotis)

Discrepancies between the census size and the genetically effective size of populations (N(e)) can be caused by a number of behavioural and demographic factors operating within populations. Specifically, strong skew in male reproductive success, as would be expected in a polygynous mating system, could cause a substantial decrease in N(e) relative to census size. Because the mating system of Neotoma macrotis had previously been described as one nearing harem polygyny, I examined the distribution of reproductive success and genetic variation within a population of this species. Combining genetic data and three years of field observations, I show that variance in reproductive success does not deviate from poisson expectations within either sex and variance in success is similar between the sexes. Furthermore, both males and females had multiple partners across litters in addition to some evidence of multiple paternity within litters. Despite a lack of strong skew in reproductive success, an estimate of N(e) based on a number of demographic parameters suggests that the ratio of N(e)/N in this population is 0.48. Although the ratio of N(e)/N suggests that the population is experiencing higher rates of genetic drift than would be expected based on census size alone, the population maintains high levels of genetic diversity. Estimates of neighbourhood size and patterns of recruitment to the study site suggest that immigration plays an important role in this population and may contribute to the maintenance of high levels of genetic diversity.     

Genetic consequences of polygyny and social structure in an Indian fruit bat, Cynopterus sphinx. I. Inbreeding, outbreeding, and population subdivision

Population subdivision into behaviorally cohesive kin groups influences rates of inbreeding and genetic drift and has important implications for the evolution of social behavior. Here we report the results of a study designed to test the hypothesis that harem social structure promotes inbreeding and genetic subdivision in a population with overlapping generations. Genetic consequences of harem social structure were investigated in a natural population of a highly polygynous fruit bat, Cynopterus sphinx (Chiroptera: Pteropodidae), in western India. The partitioning of genetic variance within and among breeding groups was assessed using 10-locus microsatellite genotypes for 431 individually marked bats. Genetic analysis of the C. sphinx study population was integrated with field data on demography and social structure to determine the specific ways in which mating, dispersal, and new social group formation influenced population genetic structure. Microsatellite data revealed striking contrasts in genetic structure between consecutive offspring cohorts and between generations. Relative to the 1998 (dry-season) offspring cohort, the 1997 (wet-season) cohort was characterized by a more extensive degree of within-group heterozygote excess (F(IS) = -0.164 vs. -0.050), a greater degree of among-group subdivision (F(ST) = 0.123 vs. 0.008), and higher average within-group relatedness (r = 0.251 vs. 0.017). Differences in genetic structure between the two offspring cohorts were attributable to seasonal differences in the number and proportional representation of male parents. Relative to adult age-classes, offspring cohorts were characterized by more extensive departures from allelic and genotypic equilibria and a greater degree of genetic subdivision. Generational differences in F-statistics indicated that genetic structuring of offspring cohorts was randomized by natal dispersal prior to recruitment into the breeding population. Low relatedness among harem females (r = 0.002-0.005) was primarily attributable to high rates of natal dispersal and low rates of juvenile survivorship. Kin selection is therefore an unlikely explanation for the formation and maintenance of behaviorally cohesive breeding groups in this highly social mammal.     

The effects of cyclic dynamics and mating system on the effective size of an island mouflon population

The Haute Island mouflon (Ovis aries) population is isolated on one small (6.5 km2) island of the remote Kerguelen archipelago. Given a promiscuous mating system, a cyclic demography and a strong female-biased sex ratio after population crashes, we expected a low effective population size (Ne). We estimated Ne using demographic and temporal genetic approaches based on genetic information at 25 microsatellite loci from 62 and 58 mouflons sampled in 1988 and 2003, respectively. Genetic Ne estimates were higher than expected, varying between 104 and 250 depending on the methods used. Both demographic and genetic approaches show the Haute Island Ne is buffered against population crashes. The unexpectedly high Ne likely results from the cyclic winter crashes that allow young males to reproduce, limiting the variance of male reproductive success. Based on individual-based simulations, we suggest that despite a strongly female-biased sex ratio, the effects of the mating system on the effective population size more closely resemble random mating or weak polygyny.     

Variance in Female Reproductive Success Differentially Impacts Effective Population Size in the Short-Nosed Fruit Bat, <Emphasis Type="Italic">Cynopterus sphinx</Emphasis>

Effective population size (N _e) quantifies the effects of micro-evolutionary processes and the rate of loss of genetic diversity in a population. Several demographic and mating parameters reduce N _e. Theoretical studies elucidate the impacts of various demographic and mating system parameters on N _e, while empirical studies illustrate realized N _e for species with differing life histories and mating systems. However, effect of intra-specific variation in mating system on effective size remains largely unexplored. In this paper we investigated the effect of promiscuous and polygynous mating on N _e in two wild populations of the short-nosed fruit bat, Cynopterus sphinx. N _e/N (ratio of effective population size to census size) was lower than unity in both populations, and much lower for the polygynous population compared to promiscuous population. Elasticity analyses reveal that N _e/N was sensitive to deviations in the sex ratio. Variance in female reproductive success had a higher impact on N _e compared to variance in male reproductive success in the promiscuous population. However, for the polygynous population, impact of variance in male reproductive success on N _e was higher than that of variance in female reproductive success. Our results suggest that depending on mating system, different populations of the same species could have alternate evolutionary trajectories. The rate of loss of genetic diversity would be lower for the promiscuous population compared to the polygynous population. Our study is the first to highlight which parameters would most significantly impact population specific N _e under different mating systems.     

Promiscuous mating in the harem-roosting fruit bat, Cynopterus sphinx

Observations on mating behaviours and strategies guide our understanding of mating systems and variance in reproductive success. However, the presence of cryptic strategies often results in situations where social mating system is not reflective of genetic mating system. We present such a study of the genetic mating system of a harem-forming bat Cynopterus sphinx where harems may not be true indicators of male reproductive success. This temporal study using data from six seasons on paternity reveals that social harem assemblages do not play a role in the mating system, and variance in male reproductive success is lower than expected assuming polygynous mating. Further, simulations reveal that the genetic mating system is statistically indistinguishable from promiscuity. Our results are in contrast to an earlier study that demonstrated high variance in male reproductive success. Although an outcome of behavioural mating patterns, standardized variance in male reproductive success (I(m)) affects the opportunity for sexual selection. To gain a better understanding of the evolutionary implications of promiscuity for mammals in general, we compared our estimates of I(m) and total opportunity for sexual selection (I(m) /I(f), where I(f) is standardized variance in female reproductive success) with those of other known promiscuous species. We observed a broad range of I(m) /I(f) values across known promiscuous species, indicating our poor understanding of the evolutionary implications of promiscuous mating.     

Estimation of genetically effective breeding numbers using a rejection algorithm approach

Polygynous mating results in nonrandom sampling of the adult male gamete pool in each generation, thereby increasing the rate of genetic drift. In principle, genetic paternity analysis can be used to infer the effective number of breeding males (Nebm). However, this requires genetic data from an exhaustive sample of candidate males. Here we describe a new approach to estimate Nebm using a rejection algorithm in association with three statistics: Euclidean distance between the frequency distributions of maternally and paternally inherited alleles, average number of paternally inherited alleles and average gene diversity of paternally inherited alleles. We quantify the relationship between these statistics and Nebm using an individual-based simulation model in which the male mating system varied continuously between random mating and extreme polygyny. We evaluate this method using genetic data from a natural population of highly polygynous fruit bats (Cynopterous sphinx). Using data in the form of mother-offspring genotypes, we demonstrate that estimates of Nebm are very similar to independent estimates based on a direct paternity analysis that included data on candidate males. Our method also permits an evaluation of uncertainty in estimates of Nebm and thus facilitates inferences about the mating system from genetic data. Finally, we investigate the sensitivity of our method to sample size, model assumptions, adult population size and the mating system. These analyses demonstrate that the rejection algorithm provides accurate estimates of Nebm across a broad range of demographic scenarios, except when the true Nebm is high.     

Demographic and genetic estimates of effective population size (Ne) reveals genetic compensation in steelhead trout

Estimates of effective population size (Ne) are required to predict the impacts of genetic drift and inbreeding on the evolutionary dynamics of populations. How the ratio of Ne to the number of sexually mature adults (N) varies in natural vertebrate populations has not been addressed. We examined the sensitivity of Ne/N to fluctuations of N and determined the major variables responsible for changing the ratio over a period of 17 years in a population of steelhead trout (Oncorhynchus mykiss) from Washington State. Demographic and genetic methods were used to estimate Ne. Genetic estimates of Ne were gained via temporal and linkage disequilibrium methods using data from eight microsatellite loci. DNA for genetic analysis was amplified from archived smolt scales. The Ne/N from 1977 to 1994, estimated using the temporal method, was 0.73 and the comprehensive demographic estimate of Ne/N over the same time period was 0.53. Demographic estimates of Ne indicated that variance in reproductive success had the most substantial impact on reducing Ne in this population, followed by fluctuations in population size. We found increased Ne/N ratios at low N, which we identified as genetic compensation. Combining the information from the demographic and genetic methods of estimating Ne allowed us to determine that a reduction in variance in reproductive success must be responsible for this compensation effect. Understanding genetic compensation in natural populations will be valuable for predicting the effects of changes in N (i.e. periods of high population density and bottlenecks) on the fitness and genetic variation of natural populations.     

OPPORTUNITY FOR SEXUAL SELECTION AND EFFECTIVE POPULATION SIZE IN THE LEK-BREEDING EUROPEAN TREEFROG (HYLA ARBOREA).

Sexual selection in lek-breeding species might drastically lower male effective population size, with potentially important consequences for evolutionary and conservation biology. Using field-monitoring and parental-assignment methods, we analyzed sex-specific variances in breeding success in a population of European treefrogs, to (1) help understanding the dynamics of genetic variance at sex-specific loci, and (2) better quantify the risk posed by genetic drift in this species locally endangered by habitat fragmentation. The variance in male mating success turned out to be markedly lower than values obtained from other amphibian species with polygamous mating systems. The ratio of effective breeding size to census breeding size was only slightly lower in males (0.44) than in females (0.57), in line with the patterns of genetic diversity previously reported from H. arborea sex chromosomes. Combining our results with data on age at maturity and adult survival, we show that the negative effect of the mating system is furthermore compensated by the effect of delayed maturity, so that the estimated instantaneous effective size broadly corresponded to census breeding size. We conclude that the lek-breeding system of treefrogs impacts only weakly the patterns of genetic diversity on sex-linked genes and the ability of natural populations to resist genetic drift.     

Effects of Partial Inbreeding on Fixation Rates and Variation of Mutant Genes

Diffusion methods were used to investigate the fixation probability, average time until fixation and extinction, and cumulative heterozygosity and genetic variance for single mutant genes in finite populations with partial inbreeding. The critical parameters in the approximation are the coefficient of inbreeding due to nonrandom mating (F) and the effective population size (Ne), which also depends on F and the variance of family size. For large Ns, the fixation probability (u) is u = 2(Ne/N)s (F + h - Fh), where N is the population census, s is the coefficient of selection of the mutant homozygote and h is the coefficient of dominance. For Poisson family size (independent Poisson distributions of selfed and nonselfed offspring with partial selfing, and independent Poisson distributions of male and female numbers with partial sib mating), Ne = N/(1 + F), and the time until fixation is approximately equal to Ne/N times the time to fixation with random mating, but this relation does not hold, however, for other distributions of family size. The cumulative nonadditive variance until fixation or loss for dominant genes is reduced with increasing F while for recessive genes it is increased with intermediate values of F. The average time until extinction of deleterious mutations is reduced by increasing F. This reduction, when expressed as a proportion, is approximately independent of the initial gene frequency as well as the selective disadvantage if this is large.     

Parentage, reproductive success and breeding behaviour in the greater horseshoe bat (Rhinolophus ferrumequinum)

Female greater horseshoe bats form maternity colonies each summer in order to give birth and raise young. During the mating period, females visit males occupying territorial sites, copulation takes place and sperm are stored until ovulation occurs, normally in April. Using microsatellite markers and a likelihood method of parentage analysis, we studied breeding behaviour and male reproductive success over a five-year period in a population of bats in south-west Britain. Paternity was assigned with 80% confidence to 44% of young born in five successive cohorts. While a small annual skew in male reproductive success was detected, the variance increased over five years due to the repeated success of a few individuals. Mating was polygynous, although some females gave birth to offspring sired by the same male in separate years. Such repeated partnerships probably result from fidelity for either mating sites or individuals or from sperm competition. Females mated with males born both within and outside their own natal colony; however, relatedness between parents was no less than the average recorded for male female pairs. Gene flow between colonies is likely to be primarily mediated by both female and male dispersal during the mating period rather than more permanent movements.     

Correlates of male reproductive success in Padogobius martensi (Gobiidae)

Factors affecting male reproductive success were investigated in a natural population of Padogobius martensi , a small freshwater goby showing paternal care. Males were found to be polygynous and their mating success was related both to their body length and to the size of the nest occupied. Body size was a good predictor for the presence of eggs in the nest. The number of egg batches guarded by a male was highly correlated with the area of his nest. Mature males with a total length of 48 mm or less (1-year-old individuals) occupied nest sites in breeding areas but were never found with eggs in their nests. The components of sexual selection which may determine the variance in mating success are discussed.     

Effective size of two feral domestic cat populations (Felis catus L): effect of the mating system

A variety of behavioural traits have substantial effects on the gene dynamics and genetic structure of local populations. The mating system is a plastic trait that varies with environmental conditions in the domestic cat (Felis catus) allowing an intraspecific comparison of the impact of this feature on genetic characteristics of the population. To assess the potential effect of the heterogenity of males' contribution to the next generation on variance effective size, we applied the ecological approach of Nunney & Elam (1994) based upon a demographic and behavioural study, and the genetic 'temporal methods' of Waples (1989) and Berthier et al. (2002) using microsatellite markers. The two cat populations studied were nearly closed, similar in size and survival parameters, but differed in their mating system. Immigration appeared extremely restricted in both cases due to environmental and social constraints. As expected, the ratio of effective size to census number (Ne/N) was higher in the promiscuous cat population (harmonic mean = 42%) than in the polygynous one (33%), when Ne was calculated from the ecological method. Only the genetic results based on Waples' estimator were consistent with the ecological results, but failed to evidence an effect of the mating system. Results based on the estimation of Berthier et al. (2002) were extremely variable, with Ne sometimes exceeding census size. Such low reliability in the genetic results should retain attention for conservation purposes.     

Effective Size of Nonrandom Mating Populations

Nonrandom mating whereby parents are related is expected to cause a reduction in effective population size because their gene frequencies are correlated and this will increase the genetic drift. The published equation for the variance effective size, Ne, which includes the possibility of nonrandom mating, does not take into account such a correlation, however. Further, previous equations to predict effective sizes in populations with partial sib mating are shown to be different, but also incorrect. In this paper, a corrected form of these equations is derived and checked by stochastic simulation. For the case of stable census number, N, and equal progeny distributions for each sex, the equation is [formula: see text], where Sk2 is the variance of family size and alpha is the departure from Hardy-Weinberg proportions. For a Poisson distribution of family size (Sk2 = 2), it reduces to Ne = N/(1 + alpha), as when inbreeding is due to selfing. When nonrandom mating occurs because there is a specified system of partial inbreeding every generation, alpha can be substituted by Wright's FIS statistic, to give the effective size as a function of the proportion of inbred mates.     

Individual reproductive success and effective population size in the greater white-toothed shrew Crocidura russula

In order to investigate the determinants of effective population size in the socially monogamous Crocidura russula, the reproductive output of 44 individuals was estimated through genetic assignment methods. The individual variance in breeding success turned out to be surprisingly high, mostly because the males were markedly less monogamous than expected from previous behavioural data. Males paired simultaneously with up to four females and polygynous males had significantly more offspring than monogamous ones. The variance in female reproductive success also exceeded that of a Poisson distribution (though to a lesser extent), partly because females paired with multiply mated males weaned significantly more offspring. Polyandry also occurred occasionally, but only sequentially (i.e. without multiple paternity of litters). Estimates of the effective to census size ratio were ca. 0.60, which excluded the mating system as a potential explanation for the high genetic variance found in this shrew's populations. Our data suggest that gene flow from the neighbourhood (up to one-third of the total recruitment) is the most likely cause of the high levels of genetic diversity observed in this shrew's subpopulations.     

Weak polygyny in California sea lions and the potential for alternative mating tactics

Female aggregation and male territoriality are considered to be hallmarks of polygynous mating systems. The development of genetic parentage assignment has called into question the accuracy of behavioral traits in predicting true mating systems. In this study we use 14 microsatellite markers to explore the mating system of one of the most behaviorally polygynous species, the California sea lion (Zalophus californianus). We sampled a total of 158 female-pup pairs and 99 territorial males across two breeding rookeries (San Jorge and Los Islotes) in the Gulf of California, Mexico. Fathers could be identified for 30% of pups sampled at San Jorge across three breeding seasons and 15% of sampled pups at Los Islotes across two breeding seasons. Analysis of paternal relatedness between the pups for which no fathers were identified (sampled over four breeding seasons at San Jorge and two at Los Islotes) revealed that few pups were likely to share a father. Thirty-one percent of the sampled males on San Jorge and 15% of the sampled males on Los Islotes were assigned at least one paternity. With one exception, no male was identified as the father of more than two pups. Furthermore, at Los Islotes rookery there were significantly fewer pups assigned paternity than expected given the pool of sampled males (p<0.0001). Overall, we found considerably lower variation in male reproductive success than expected in a species that exhibits behavior associated with strongly polygynous mating. Low variation in male reproductive success may result from heightened mobility among receptive females in the Gulf of California, which reduces the ability of males to monopolize groups of females. Our results raise important questions regarding the adaptive role of territoriality and the potential for alternative mating tactics in this species.     

Estimation of effective population size for the long-lived darkblotched rockfish Sebastes crameri

We report the variance effective population size (Ne) in darkblotched rockfish (Sebastes crameri) utilizing the temporal method for overlapping generations, which requires a combination of age-specific demography and genetic information from cohorts. Following calculations of age-specific survival and reproductive success from fishery data, we genotyped a sample (n = 1087) comprised by 6 cohorts (from 1995 to 2000) across 7 microsatellite loci. Our Ne estimate (Ne) plus 95% confidence interval was (Ne) = 9157 [6495-12 215], showing that the breeding population number could be 3-4 orders of magnitude smaller than the census population size (N) = 24 376 210). Our estimates resemble closely those found for fishes with similar life history, suggesting that the small (Ne)/(N) ratio for S. crameri is most likely explained by a combination of high variance in reproductive success among individuals, genetic structure, and demographic perturbations such as historical fishing. Because small (Ne)/(N) ratios have been commonly associated with potential loss of genetic variation, our estimates need careful consideration in rockfish management and conservation.     

The influence of age structure and fecundity on effective population size.

Simple formulae are developed which define the effective size (Ne) of populations with overlapping generations, and their use is illustrated using data from a squirrel population. Two mating systems are considered, the random union of gametes and monogamy, in combination with age-independent fecundity. In the simplest case of age-independent (type 2) survivorship in a population of N adults, Ne = N/(2-T-1) where T is the generation time. As T increases, Ne declines asymptomatically to N/2. A generalization of this result (Ne = N/[1 + k-1-T-1], where k influences survivorship) shows that given type 1 survivorship (k greater than 1) this decline in Ne is less severe. A biased sex ratio results in Ne differing between the two mating systems; however, in both systems, a sex ratio bias resulting from survival differences has much less influence on Ne than a sex ratio bias resulting from recruitment differences. Low fecundity can increase Ne, but realistic levels of variation among breeding individuals (Poisson or greater) negate the effect. The effect on Ne of variation resulting from the presence of non-breeders is also considered.     

Mating system, sexual dimorphism, and the opportunity for sexual selection in a territorial ungulate

In mammals, species with high sexual size dimorphism tend tohave highly polygynous mating systems associated with high variancein male lifetime reproductive success (LRS), leading to a highopportunity for sexual selection. However, little informationis available for species with weak sexual size dimorphism. Ina long-term study population, we used parentage analysis basedon 21 microsatellite markers to describe, for the first time,variance in male lifetime breeding success (LBS) of roe deer,a territorial ungulate where males weigh less than 10% morethan females. LBS ranged from 0 to 14 (mean = 4.54, variance= 15.5), and its distribution was highly skewed, with only afew males obtaining high LBS and many males failing to breedor siring only one fawn. As predicted for polygynous specieswith low sexual size dimorphism, the standardized variance inmale LBS was low (I_m = 0.75) and was only slightly higher thanthe standardized variance in female LRS (I_f = 0.53), suggestinga low opportunity for sexual selection. The I_m value reportedhere for roe deer is much lower than values reported for highlydimorphic ungulates such as red deer (I_m > 3). We suggestthat, along a continuum of opportunity for sexual selection,roe deer occupy a position closer to monogamous and monomorphicterritorial ungulates than to highly polygynous, sexually dimorphicungulates with dominance rank–based mating systems suchas harems or roving mating systems.     

Polygyny and nest site selection in the pied flycatcher

Nest site choice, and its influence on mating and breeding success were studied in a population of individually marked pied flycatchers (Ficedula hypoleuca) for 7 years. Some nest boxes were used more frequently than expected from random choice of nest site. Flycatchers bred more successfully in such attractive boxes, irrespective of whether the brood was attended by the male or not. Arriving males and females settled at boxes in descending order of attractiveness. Boxes accepted by females were more attractive than alternative boxes advertised simultaneously by males. Secondary nest boxes of polygynous males tended to be more attractive than boxes at which monogamous males displayed, without success, for secondary mates. Returning males with local breeding experience started to sing at nest boxes earlier in spring than first season males, settled at more attractive boxes, and mated polygynously more often. The results indicate that male mating success should be closely dependent on the male's ability to monopolize attractive nest sites.     

EVOLUTION,PHYLOGENY, SEXUAL DIMORPHISM AND MATING SYSTEM IN THE GRACKLES (QUISCALUS SPP.: ICTERINAE)

According to theory, two consequences of sexual selection are sexual dimorphism in size and secondary sexual characteristics, due to either intra- or intersexual selection. In this paper I suggest three criteria for the test of an evolutionary hypothesis involving quantitative morphological characters. First, the postulated change must be shown to have occurred in evolutionary time. Second, this change must be positively correlated with a change in the proposed selective agent. Third, given two taxa with different degrees of sexual size dimorphism and different mating system, the possible influence of drift must be rejected. If the hypothesis is not rejected by these three criteria, then we still have no proof of causality, but we can at least be more confident about its plausibility. This is applied to the particular hypothesis that sexual dimorphism in the Boat-tailed and Great-tailed grackles (Quiscalus spp; Icterinae; Aves) is caused by the highly polygynous mating system in these species. In relation to an outgroup, both species have increased disproportionately in male tarsus and tail size, creating an increased sexual dimorphism. This has cooccurred with the evolution of their particular mating system. However, the variance among species in male tarsus size can be accounted for by drift, and need not be a result of selection for increased size. In contrast, the variance among species in male tail size was much larger than expected under a null model of drift, indicating directional selection for long tails. The variance in female tail size was not larger than expected by drift, whereas the variance in female tarsus size was in fact lower than expected by drift, indicating stabilizing selection. The data are consistent with the hypothesis with regard to tail size, but not with regard to body size.