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Population biology of the invasive freshwater snail Physa acuta approached through genetic markers, ecological characterization and demography.

Abstract The respective role of factors acting on population functioning can be inferred from a variety of approaches, including population genetics and demography. We here investigated the role of four of these factors (mating systems, population size, bottlenecks and migration) in the hermaphroditic freshwater snail Physa acuta. Twenty-four populations were sampled either around Montpellier (local scale), or at the scale of France (global scale). At local scale, eight populations were sampled twice, before and after summer drying out. The genetic structure of these populations was studied using microsatellite loci. Populations were classified according to openness (ponds vs. rivers) and water regime (permanent vs. temporary) allowing predictions on genetic patterns (e.g. diversity within populations and differentiation). At local scale, progeny-arrays analysis of the selfing rate was conducted, and size distributions of individuals were followed over two years. Results with regard to the four factors mentioned above were: (i) Estimates of population selfing rates derived from inbreeding coefficients were only slightly higher than those from progeny-arrays. (ii) More variation was detected in rivers than in ponds, but no influence of water regime was detected. One reason might be that permanent populations are not going less often through low densities than those from temporary habitats at the time scale studied. (iii) There was limited evidence for genetic bottlenecks which is compatible with the fact that even marked reduction in water availability was not necessarily associated with demographic bottlenecks. More generally, bottlenecks reducing genetic variation probably occur at population foundation. (iv) Lower genetic differentiation was detected among rivers than among ponds which might be related to limitations on gene flow. Demographic and temporal genetic data further indicates that flooding in rivers is unlikely to induce marked gene flow explaining the strong genetic differentiation at short geographical scale in such habitats. Finally, the demographic data suggest that some populations are transitory and subject to recurrent recolonization, a pattern that was also detected through genetic data.

Animals↗

Temporal changes in allele frequencies and low effective population size in greater prairie-chickens.

The number of greater prairie-chickens in Wisconsin has decreased by 91% since 1932. The current population of approximately 1500 birds exists primarily in four isolated management areas. In previous studies of the Wisconsin populations we documented low levels of genetic variation at microsatellite loci and the mitochondrial DNA control region. Here we investigate changes in genetic structure between the four management areas in Wisconsin over the last 50 years. We estimated the harmonic mean effective population size (Ne) over the last 50 years by comparing allele frequencies from the early 1950s with those from contemporary samples. Using a pseudo-likelihood approach that accounted for migration, estimates of Ne (15-32 prairie-chickens within each management area) were 10 times lower than census numbers from booming-ground counts. These low estimates of Ne are consistent with increased habitat fragmentation and an increase in genetic isolation between management areas over the last 50 years. The reduction of gene flow between areas has reduced Ne, increased genetic drift and, consequently, reduced genetic variation. These results have immediate consequences for the conservation of the prairie-chicken, and highlight the importance of how mating systems and limited dispersal may exacerbate the loss of genetic variation in fragmented populations.

Animals↗

Sex-specific correlation between heterozygosity and clone size in the trematode Schistosoma mansoni.

The mode of reproduction (sexual and/or asexual) and the mating system determine the patterns of gene transmission and genotype formation across generations. Schistosoma mansoni is a dioecious trematode that necessarily alternates sexual and asexual reproduction during its life cycle. In a previous study of the distribution of S. mansoni genetic variability within and between definitive host individuals, we noticed that deleting multilocus genotypes from each infrapopulation so as to keep only one copy of each multilocus genotype, seemed to have a substantial effect on FIS values. More precisely, female FIS increased when repeated genotypes were removed whereas no effect was observed on male FIS. This suggested that multilocus genotypes at high frequency tended to be more heterozygous. The aim of the present study is specifically to test and analyse this phenomenon. We demonstrate that the number of repetitions per clone correlates with individual heterozygosity. This effect is however, sex-specific: only female clone size correlates with heterozygosity. We discuss this phenomenon in relation to the heterozygosity-fitness relationship and the sex-specific response to inbreeding depression.

Animals↗

Spatial structure of genetic variation and primary succession in the pioneer tree species Antirhea borbonica on La Réunion.

In habitats where colonization and extinction are recurrent, the distribution of gene frequencies among patches of suitable habitat may reflect the age structure of different populations. In this study, we quantify population genetic structure for a pioneer tree species, Antirhea borbonica, in a chrono-sequence of primary succession on the lava flows of the Piton de La Fournaise volcano (La Réunion). Using microsatellite loci and amplified fragment length polymorphism (AFLP) markers, we quantified genetic variation within and among populations for early- and late-succession populations in a landscape where extinction and recolonization are recurrent (the 'Grand Brûlé') and for late-succession populations in a more stable landscape. This study produced three main results. First, we detected no evidence that founder events increase genetic differentiation among colonizing populations; F(ST) values among early- and among late-succession populations were similar. Second, we found no evidence for isolation by distance; genetic distance was not correlated with spatial distance within and among populations. Third, F(IS) values are consistently high in all populations, despite the fact that A. borbonica populations are functionally close to dioecy and thus expected to have an outcrossing mating system. Multiple colonization events from different sources may limit differentiation among young populations and spatial isolation may enhance differentiation among late-succession populations. Ecological processes acting during colonization may create the conditions for spatial aggregation within pioneer populations, and thus contribute to the high F(IS) values.

DNA Primers↗

Parentage versus two-generation analyses for estimating pollen-mediated gene flow in plant populations.

Assessment of contemporary pollen-mediated gene flow in plants is important for various aspects of plant population biology, genetic conservation and breeding. Here, through simulations we compare the two alternative approaches for measuring pollen-mediated gene flow: (i) the NEIGHBORHOOD model--a representative of parentage analyses, and (ii) the recently developed TWOGENER analysis of pollen pool structure. We investigate their properties in estimating the effective number of pollen parents (N(ep)) and the mean pollen dispersal distance (delta). We demonstrate that both methods provide very congruent estimates of N(ep) and delta, when the methods' assumptions considering the shape of pollen dispersal curve and the mating system follow those used in data simulations, although the NEIGHBORHOOD model exhibits generally lower variances of the estimates. The violations of the assumptions, especially increased selfing or long-distance pollen dispersal, affect the two methods to a different degree; however, they are still capable to provide comparable estimates of N(ep). The NEIGHBORHOOD model inherently allows to estimate both self-fertilization and outcrossing due to the long-distance pollen dispersal; however, the TWOGENER method is particularly sensitive to inflated selfing levels, which in turn may confound and suppress the effects of distant pollen movement. As a solution we demonstrate that in case of TWOGENER it is possible to extract the fraction of intraclass correlation that results from outcrossing only, which seems to be very relevant for measuring pollen-mediated gene flow. The two approaches differ in estimation precision and experimental efforts but they seem to be complementary depending on the main research focus and type of a population studied.

Computer Simulation↗

Unbiased estimation of relative reproductive success of different groups: evaluation and correction of bias caused by parentage assignment errors.

Parentage assignment is widely applied to studies on mating systems, population dynamics and natural selection. However, little is known about the consequence of assignment errors, especially when some parents are not sampled. We investigated the effects of two types of error in parentage assignment, failing to assign a true parent (type A) and assigning an untrue parent (type B), on an estimate of the relative reproductive success (RRS) of two groups of parents. Employing a mathematical approach, we found that (i) when all parents are sampled, minimizing either type A or type B error insures the minimum bias on RRS, and (ii) when a large number of parents is not sampled, type B error substantially biases the estimated RRS towards one. Interestingly, however, (iii) when all parents were sampled and both error rates were moderately high, type A error biased the estimated RRS even more than type B error. We propose new methods to obtain an unbiased estimate of RRS and the number of offspring whose parents are not sampled (zW(z)), by correcting the error effects. Applying them to genotypic data from steelhead trout (Oncorhynchus mykiss), we illustrated how to estimate and control the assignment errors. In the data, we observed up to a 30% assignment error and a strong trade-off between the two types of error, depending on the stringency of the assignment decision criterion. We show that our methods can efficiently estimate an unbiased RRS and zW(z) regardless of assignment method, and how to maximize the statistical power to detect a difference in reproductive success between groups.

Animals↗

A tale of two siblings: multiple paternity in big brown bats (Eptesicus fuscus) demonstrated using microsatellite markers.

In many bat species, the opportunity for sperm competition or other mechanisms of post-copulatory paternity biasing is thought to be great, due to the long delay between copulation and fertilization, demonstrated sperm storage capabilities, and observed promiscuity. We present the results of the first study to assess whether litters of big brown bats (Eptesicus fuscus) containing dizygotic twins share the same father. We sampled 26 mother-offspring triads from three colonies in Indiana and Illinois, as well as 299 additional adults (237 females and 62 males) from these colonies and six other maternity colonies in the same area in 1997-1998. All individuals were genotyped at nine highly variable autosomal microsatellite loci and one X-linked locus. We assessed multiple paternity using autosomal and X-linked locus exclusions, and using maximum-likelihood methods. All methods confirmed multiple paternity within litters, and the maximum-likelihood analyses indicated that almost half of the sampled litters were composed of maternal half-siblings rather than full-siblings. Our results highlight the potential importance of post-copulatory mechanisms of paternity determination in the mating system of big brown bats, and have important implications for gene flow and population structuring in this species.

Animals↗

Inferring colonization history from analyses of spatial genetic structure within populations of Pinus strobus and Quercus rubra.

Many factors interact to determine genetic structure within populations including adult density, the mating system, colonization history, natural selection, and the mechanism and spatial patterns of gene dispersal. We examined spatial genetic structure within colonizing populations of Quercus rubra seedlings and Pinus strobus juveniles and adults in an aspen-white pine forest in northern Michigan, USA. A 20-year spatially explicit demographic study of the forest enables us to interpret the results in light of recent colonization of the site for both species. We assayed 217 Q. rubra seedlings and 171 P. strobus individuals at 11 polymorphic loci using nine allozyme systems. Plant genotypes and locations were used in an analysis of spatial genetic structure. Q. rubra and P. strobus showed similar observed levels of heterozygosity, but Q. rubra seedlings have less heterozygosity than expected. Q. rubra seedlings show spatial genetic clumping of individuals on a scale to 25 m and levels of genetic relatedness expected from the clumped dispersion of half-siblings. In contrast, P. strobus has low levels of genetic relatedness at the smallest distance class and positive spatial genetic structure at scales < 10 m within the plot. The low density of adult Q. rubra outside the study plot and limited, spatially clumped rodent dispersal of acorns is likely responsible for the observed pattern of spatial genetic structure and the observed heterozygote deficit (i.e. a Wahlund effect). We attribute weaker patterns observed in P. strobus to the longer dispersal distance of seeds and the historical overlap of seed shadows from adults outside of the plot coupled with the overlap of seed shadows from younger, more recently established reproductive adults. The study demonstrates the utility of long-term demographic data in interpreting mechanisms responsible for generating contemporary patterns of genetic structure within populations.

Genetic Variation↗

Microsatellites provide insight into contrasting mating patterns in arribada vs. non-arribada olive ridley sea turtle rookeries.

Molecular studies of sea turtles have shown that the frequency of multiple paternity (MP) varies between species, and between rookeries of the same species. This study uses nuclear microsatellite markers to compare the incidence of MP in two neighbouring olive ridley rookeries on the Pacific coast of Costa Rica, with contrasting nesting behaviours -- the 'arribada' population nesting at Ostional and the solitary nesters of Playa Hermosa. Using two highly polymorphic microsatellite markers, we tested 13 nests from each location and found a significant difference (P < 0.001) between the level of MP of the arribada rookery (92%- the highest found for marine turtles) and that of the solitary nesting rookery (30%). Additional analyses based on six microsatellite loci revealed no genetic differentiation between nesting females from the two locations, or between nesting females and attendant males from the Ostional breeding area. Sixty-nine per cent of the nests with MP were fathered by a minimum of three different males, and three nests showed evidence of at least four fathers. The results suggest that the differences observed in levels of MP between arribada and solitary rookeries are due to an effect of abundance of individuals on the mating system. This is supported by a regression analysis combining other paternity studies on sea turtles which shows that levels of MP increase with increasing abundance of nesting females.

Alleles↗

Fine-scale genetic structure of life history stages in the food-deceptive orchid Orchis purpurea.

In natural plant populations, fine-scale spatial genetic structure can result from limited gene flow, selection pressures or historical events, but the role of each factor is in general hard to discern. One way to investigate the origination of spatial genetic structure within a plant population consists of comparing spatial genetic structure among different life history stages. In this study, spatial genetic structure of the food-deceptive orchid Orchis purpurea was determined across life history stages in two populations that were regenerating after many years of population decline. Based on demographic analyses (2001-2004), we distinguished between recruits and adult plants. For both sites, there was no difference in the proportion of polymorphic loci and expected heterozygosity between life history stages. However, spatial autocorrelation analyses showed that spatial genetic structure increased in magnitude with life history stage. Weak or no spatial genetic structure was observed for recruits, whereas adult plants showed a pattern that is consistent with that found in other species with a predominantly outcrossing mating system. The observed differences between seedlings and adults are probably a consequence of changes in management of the two study sites and associated demographic changes in both populations. Our results illustrate that recurrent population crashes and recovery may strongly affect genetic diversity and fine-scale spatial genetic structure of plant populations.

Flowers↗

Genetic structure at range edge: low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations.

Understanding the genetic composition and mating systems of edge populations provides important insights into the environmental and demographic factors shaping species' distribution ranges. We analysed samples of the mangrove Avicennia marina from Vietnam, northern Philippines and Australia, with microsatellite markers. We compared genetic diversity and structure in edge (Southeast Asia, and Southern Australia) and core (North and Eastern Australia) populations, and also compared our results with previously published data from core and southern edge populations. Comparisons highlighted significantly reduced gene diversity and higher genetic structure in both margins compared to core populations, which can be attributed to very low effective population size, pollinator scarcity and high environmental pressure at distribution margins. The estimated level of inbreeding was significantly higher in northeastern populations compared to core and southern populations. This suggests that despite the high genetic load usually associated with inbreeding, inbreeding or even selfing may be advantageous in margin habitats due to the possible advantages of reproductive assurance, or local adaptation. The very high level of genetic structure and inbreeding show that populations of A. marina are functioning as independent evolutionary units more than as components of a metapopulation system connected by gene flow. The combinations of those characteristics make these peripheral populations likely to develop local adaptations and therefore to be of particular interest for conservation strategies as well as for adaptation to possible future environmental changes.

Australia↗

Genetic tagging reveals extreme site fidelity in territorial male Antarctic fur seals Arctocephalus gazella.

Genetic tagging, the identification of individuals using their genotypes, provides a powerful tool for studying animals that are difficult to observe or identify using conventional techniques. However, despite being widely adopted by conservation biologists, the full potential of this approach has yet to be realized. Here we used genetic recapture data to quantify male site fidelity at a colony of Antarctic fur seals where an aerial walkway provides unprecedented access and individual positions are determined daily to 1 m accuracy. Because males are too large and aggressive to be captured and fitted with conventional tags, we remotely collected 770 tissue samples over eight consecutive seasons and used nine-locus microsatellite genotypes to reveal 306 genetic recaptures among 464 unique individuals. Within seasons, males are highly site-faithful, with any movements that occur tending to take place before the period when females come into oestrus. Of those males that return to breed over successive seasons, almost half return to within a body length of where they were before. The discovery of such extreme site faithfulness has implications for the population structure and mating system of fur seals and potentially other colonially breeding species.

Animals↗

Social group size, potential sperm competition and reproductive investment in a hermaphroditic leech, Helobdella papillornata (Euhirudinea: Glossiphoniidae).

Social group size may affect the potential for sperm competition, and this in turn may favour ontogenetic adjustments in testicular mass according to the likely requirements for sperm and spermatophore production. In a number of comparative analyses of testis mass among vertebrate species that differ in mating system or social organization, increasing potential for sperm competition is associated with larger testis size. Intraspecific phenotypic plasticity should be able to produce the same pattern if social group size is heterogenous and reflects differing degrees of average sperm competition, but this intraspecific effect is less well studied. We tested the effect of social groups on both male and female investment in the simultaneously hermaphroditic leech, Helobdella papillornata. Leeches were placed in groups of one, two, four or eight. Sexual investment at the onset of reproductive maturity was quantified as the total testisac volume for male function and total egg volume for female function. We found that testisac volume (statistically adjusted for body size) showed a significant increase with increasing group size. Total egg volume (also adjusted for body size) was unaffected by group size. Our findings indicate adaptive developmental plasticity in male gonad investment in response to the potential for sperm competition.

Animals↗

Levels of inbreeding depression over seven generations of selfing in the androdioecious clam shrimp, Eulimnadia texana.

Androdioecy (mixtures of males and hermaphrodites) is a rare mating system in both plants and animals. Theory suggests that high levels of inbreeding depression can maintain males in androdioecious populations if hermaphrodites commonly self-fertilize. However, if inbreeding depression (delta) can be 'purged' from selfing populations, maintaining males is more difficult. In the androdioecious clam shrimp, Eulimnadia texana, delta is estimated to be as high as 0.7. Previous work suggests that this high level is maintained in the face of high levels of inbreeding due to an associative overdominance of fitness-related loci with the sex-determining locus. Such associative overdominance would make purging of inbreeding depression difficult to impossible. The current experiment was designed to determine if delta can be purged in these shrimp by tracking fitness across seven generations in selfing and outcrossing treatments. Evidence of purging was found in one of four populations, but the remaining populations demonstrated a consistent pattern of delta across generations. Although the experimental design allowed ample opportunity for purging, the majority of populations were unable to purge their genetic load. Therefore, delta in this species is likely due to associative overdominance caused by deleterious recessive alleles linked to the sex determining locus.

Analysis of Variance↗

Sperm competition and the evolution of testes size in birds.

Comparative analyses suggest that a variety of ecological and behavioural factors contribute to the tremendous variability in extrapair mating among birds. In an analysis of 1010 species of birds, we examined several ecological and behavioural factors in relation to testes size; an index of sperm competition and the extent of extrapair mating. In univariate and multivariate analyses, testes size was significantly larger in species that breed colonially than in species that breed solitarily, suggesting that higher breeding density is associated with greater sperm competition. After controlling for phylogenetic effects and other ecological variables, testes size was also larger in taxa that did not participate in feeding their offspring. In analyses of both the raw species data and phylogenetically independent contrasts, monogamous taxa had smaller testes than taxa with multiple social mates, and testes size tended to increase with clutch size, which suggests that sperm depletion may play a role in the evolution of testes size. Our results suggest that traditional ecological and behavioural variables, such as social mating system, breeding density and male parental care can account for a significant portion of the variation in sperm competition in birds.

Animals↗

Thlaspi caerulescens on nonmetalliferous soil in Luxembourg: ecological niche and genetic variation in mineral element composition.

Forty-seven populations of Thlaspi caerulescens in Luxembourg were characterised for population size, soil mineral element composition and other habitat characteristics. Foliar concentrations of eight elements were assessed in 15 populations in the field and in eight populations cultivated in zinc (Zn)-cadmium (Cd)-nickel (Ni)-enriched soil. T. caerulescens favoured stony soil developed on steep, south-facing Emsian shale outcrops. All soil samples were nonmetalliferous. Soil pH ranged from 4.2 to 6.9. Field-growing plants had very high concentrations of heavy metals in the leaves (Zn, 3000-13 000 mg kg(-1); Cd, 11-44 mg kg(-1); Ni, 38-473 mg kg(-1)). Positive soil-plant correlations existed for Zn and Mn. In cultivation, significant genetic variation was found for biomass and six of eight mineral elements. For Cd and Zn, variation range among 48 half-sib families was two-fold (Cd, 183-334 mg kg(-1); Zn, 8030-16 295 mg kg(-1)). Most of the variation occurred among populations, consistent with the selfing mating system of those populations. There was a tight Zn-Cd genetic correlation (r = +0.83, P < 0.0001). The significance of the results to the conservation of T. caerulescens in Luxembourg is briefly discussed.

Ecosystem↗

A male-biased natal sex-ratio in inbred collared lemmings, Dicrostonyx groenlandicus.

A captive colony of collared lemmings (Dicrostonyx groenlandicus) from northern Alaska produced a male-biased sex ratio of 67% males for about three generations. These lemmings have a pair of autosomes fused to the sex chromosomes. Thus, males have two copies of some (formerly autosomal) sex-linked genes: One set is X-linked; the other can be described as Y-linked. Given such a karyotype, deleterious recessive alleles on the autosomal portion of the X chromosome are more resistant to selection than truly autosomal loci because they can be eliminated by homozygosity only in females. The male-bias could have resulted from one or more lethals carried on the formerly autosomal arm of the X chromosome. As inbreeding coefficients approached 0.3, the lethal was apparently homozygous in half of the homogametic (female) zygotes. This phenomenon may explain the excess of males and XY females attributed to meiotic drive in Dicrostonyx torquatus from Siberia. If under the natural mating system, inbreeding depression limits fitness, then fusion of autosomal chromatin to the sex chromosomes could be an adaptation to reduce inbreeding depression in heterogametic individuals.

Adaptation, Physiological↗

Generation of self-incompatible Arabidopsis thaliana by transfer of two S locus genes from A. lyrata.

Transitions from cross-fertilizing to self-fertilizing mating systems have occurred frequently in natural and domesticated plant populations, but the underlying genetic causes are unknown. We show that gene transfer of the stigma receptor kinase SRK and its pollen-borne ligand SCR from one S-locus haplotype of the self-incompatible and cross-fertilizing Arabidopsis lyrata is sufficient to impart self-incompatibility phenotype in self-fertile Arabidopsis thaliana, which lacks functional orthologs of these genes. This successful complementation demonstrates that the signaling cascade leading to inhibition of self-related pollen was maintained in A. thaliana. Analysis of self-incompatibility will be facilitated by the tools available in this species.

Arabidopsis↗