Similarity of contemporary and historical gene flow among highly fragmented populations of an endangered rattlesnake

Populations of endangered taxa in recently fragmented habitats often show high levels of genetic structure, but the role that contemporary versus historical processes play in generating this pattern is unclear. The eastern massasauga rattlesnake (Sistrurus c. catenatus) is an endangered snake that presently occurs throughout central and eastern North America in a series of populations that are isolated because of habitat fragmentation and destruction. Here, we use data from 19 species-specific microsatellite DNA loci to assess the levels of genetic differentiation, genetic effective population size, and contemporary and historical levels of gene flow for 19 populations sampled across the range of this snake. Eastern massasaugas display high levels of genetic differentiation (overall θ(Fst) = 0.21) and a Bayesian clustering method indicates that each population represents a unique genetic cluster even at regional spatial scales. There is a twofold variation in genetically effective population sizes but little genetic evidence that populations have undergone recent or historical declines in size. Finally, both contemporary and historical migration rates among populations were low and similar in magnitude even for populations located <7 km apart. A test of alternate models of population history strongly favours a model of long-term drift-migration equilibrium over a recent isolation drift-only model. These results suggest that recent habitat fragmentation has had little effect on the genetic characteristics of these snakes, but rather that this species has historically existed in small isolated populations that may be resistant to the long-term negative effects of inbreeding.     

Restricted gene flow in fragmented populations of a wind-pollinated tree

Fragmentation of natural populations can have negative effects at the genetic level, thus threatening their evolutionary potential. Many of the negative genetic impacts of population fragmentation can be ameliorated by gene flow and it has been suggested that in wind-pollinated tree species, high or even increased levels of gene flow are a feature of fragmented populations, although several studies have disputed this. We have used a combination of nuclear microsatellites and allele-specific PCR (AS-PCR) analysis of chloroplast single nucleotide polymorphisms (SNPs) to examine the levels and patterns of genetic diversity and population differentiation in fragmented populations of juniper (Juniperus communis) in Ireland and inform conservation programs for the species. Significant population differentiation was found for both chloroplast and nuclear markers, indicating restricted gene flow, particularly over larger geographic scales. For conservation purposes, the existence of genetically distinct clusters and geographically localised chloroplast haplotypes suggests that the concept of provenance should be taken into account when formulating augmentation or reintroduction strategies. Furthermore, the potential lack of seed dispersal and seedling establishment means that ex-situ approaches to seed and seedling management may have to be considered.     

Linking habitat use to range expansion rates in fragmented landscapes: a metapopulation approach

Temperature increases because of climate change are expected to cause expansions at the high latitude margins of species distributions, but, in practice, fragmented landscapes act as barriers to colonization for most species. Understanding how species distributions will shift in response to climate change therefore requires techniques that incorporate the combined effects of climate and landscape‐scale habitat availability on colonization rates. We use a metapopulation model (Incidence Function Model, IFM) to test effects of fine‐scale habitat use on patterns and rates of range expansion by the butterfly Hesperia comma. At its northern range margin in Britain, this species has increased its breadth of microhabitat use because of climate warming, leading to increased colonization rates. We validated the IFM by reconstructing expansions in five habitat networks between 1982 and 2000, before using it to predict metapopulation dynamics over 100 yr, for three scenarios based on observed changes to habitat use. We define the scenarios as “cold‐world” (only hot, south‐facing 150–250° hillsides are deemed warm enough), “warm‐world” in which 100–300° hillsides can be populated, and “hot‐world”, where the background climate is warm enough to enable use of all aspects (as increasingly observed). In the simulations, increased habitat availability in the hot‐world scenario led to faster range expansion rates, and to long‐term differences in distribution size and pattern. Thus, fine‐scale changes in the distribution of suitable microclimates led to landscape‐scale changes in population size and colonization rate, resulting in coarse‐scale changes to the species distribution. Despite use of a wider range of habitats associated with climate change, H. comma is still expected to occupy a small fraction of available habitat in 100 yr. The research shows that metapopulation models represent a potential framework to identify barriers to range expansion, and to predict the effects of environmental change or conservation interventions on species distributions and persistence.     

Microsatellite variation within and among recently fragmented populations of the golden lion tamarin (Leontopithecus rosalia)

Four variable microsatellite loci were used toexamine the genetic diversity and differentiation of golden lion tamarins (Leontopithecus rosalia) in four populations recently isolated by habitat fragmentation. Using Rst estimates of genetic differentiation, a considerable genetic divergence was detected among these populations, with an averagedifferentiation of 31%. Significant differences in allele number among these populations were found. However, the heterozygosity among these populations was not statistically different. These results suggestthat loss in allele diversity was faster than loss in heterozygosity. Conservation implications, particularly for golden lion tamarins, are then discussed. Loss of allelic diversity might be as serious a concern to endangered species as heterozygosity or inbreeding.     

Evidence for ancient genetic subdivision among recently fragmented populations of the endangered shrub Grevillea caleyi (Proteaceae)

The genetic effects of population fragmentation cannot be interpreted without understanding the underlying pattern of genetic variation resulting from historic population processes. We used AFLP markers to determine genetic structure and distribution of genetic diversity among populations of an endangered Australian shrub Grevillea caleyi (Proteaceae). Populations that occurred historically on four ridges have new been fragmented to varying degrees, producing some large, relatively pristine populations and very small populations consisting of fewer than 10 adult plants. We found marked population genetic structure (65.9% of genetic variation was among populations) and a significant relationship between genetic and geographic distance (rm=0.564, P=0.004). However, only 14% of overall genetic differentiation was attributable to variation among ridges, compared with 52% among populations within ridges. Moreover, genetic diversity within samples of plants did not vary with either population size or degree of isolation. Thus, the present genetic structure of populations is probably almost entirely the product of historical events. Fine-scale structuring within populations prior to fragmentation may have been caused by limited seed and pollen dispersal, despite a complex suite of (mostly avian) pollinators, and a mixed mating system that allows a large amount of selfing. The combined effects of adult longevity and a soil-stored seed bank may have buffered the recently fragmented populations against the effects of dramatic reductions in numbers of adult plants.     

Brooding crustaceans in a highly fragmented habitat: the genetic structure of Mediterranean marine cave-dwelling mysid populations

Habitat fragmentation and climate change are two major threats on biodiversity. Fragmentation limits the number of patches and their decreased connectivity cannot always maintain populations at dynamic equilibrium. The natural extreme fragmentation of marine cave habitats represents an opportunity to understand how these processes interact. The hypothesis of a low gene flow among populations due to a high level of fragmentation was tested by analysing sequence variation in a fragment of the mitochondrial gene of the cytochrome oxidase subunit I in 170 individuals (23 localities across the NW Mediterranean) of two marine cave-dwelling mysids of the genus Hemimysis. The species Hemimysis margalefi recently replaced its congener Hemimysis speluncola, a species shift that could be related to the warming of the Mediterranean Sea and to differences in their thermal tolerances. There were too few H. speluncola samples to further discuss their genetic structuring, but for H. margalefi, the present study revealed high levels of genetic diversity and genetic structuring, as shown by the eight genetically distinct groups identified. The Croatian group might constitute a sibling species due to a strong divergence (15%). Nevertheless, these groups present reduced but orientated gene flow according to the general circulation in the Mediterranean, and fit a stepping-stone model. At local scale (Marseille area, France), gene flow among caves is dependent on unexpected local hydrodynamic barriers, that determine metapopulation sizes. Through the example of mysid species inhabiting marine caves, the present work confirms the strong influence of habitat disjunction (natural fragmentation) on population structure, and stresses the importance of coastal geomorphological features in inducing complex interactions between the circulation of water masses and the circulation of genes.     

Foraging in agricultural fields: local ‘sit-and-move’ strategy scales up to risk-averse habitat use in a wolf spider

By making field observations on the movement pattern of the agrobiont wolf spider Pardosa agrestis at two spatiotemporal scales, we explored how fine-scale foraging movements scale up to medium-scale habitat use by the spiders. For fine-scale observations, we followed individuals for several metres and for up to 1-2 h. For medium-scale observations we used marking and recapture in live-trapping pitfall grids, which allowed us to detect movements up to 70 m and for 4 weeks. The analysis of fine-scale movement indicated that spiders followed a ‘sit-and-move’ foraging strategy, which consisted of variable periods of waiting (mean 2.5 min) and brief bouts of movements between the waiting sites. Spiders spent over 90% of the total observation time waiting. Prey capture (or capture attempts) was initiated only from waiting sites. Movement between consecutive waiting sites was more directional than predicted by the correlated random walk model. At medium (2-day) timescales the mean displacement of marked spiders was 7.4 m. Simulations suggested that such a displacement could be achieved if movement observed at the fine scale followed a random path for 2 days. We concluded that movement became less directional with increasing scale. Such a phenomenon might be related to avoidance of revisiting food patches locally and an efficient sampling of the habitat at higher scales. High movement activity in a species that is primarily adapted to ephemeral habitats might increase its likelihood of colonizing new habitat patches. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.     

Genetic structure of the northwestern Russian wolf populations and gene flow between Russia and Finland

We examined the genetic diversity and structure of wolf populations in northwestern Russia. Populations in Republic of Karelia and Arkhangelsk Oblast were sampled during 1995–2000, and 43 individuals were genotyped with 10 microsatellite markers. Moreover, 118 previously genotyped wolves from the neighbouring Finnish population were used as a reference population. A relatively large amount of genetic variation was found in the Russian populations, and the Karelian wolf population tended to be slightly more polymorphic than the Arkhangelsk population. We found significant inbreeding (F = 0.094) in the Karelian, but not in the Arkhangelsk population. The effective size estimates of the Karelian wolf population based on the approximate Bayesian computation and linkage disequilibrium methods were 39.9 and 46.7 individuals, respectively. AMOVA-analysis and exact test of population differentiation suggested clear differentiation between the Karelian, Arkhangelsk and Finnish wolf populations. Indirect estimates of gene flow based on the level of population differentiation (ϕ _ST  = 0.152) and frequency of private alleles (0.029) both suggested a low level of gene flow between the populations (Nm = 1.4 and Nm = 3.7, respectively). Assignment analysis of Karelian and Finnish populations suggested an even lower number of recent migrants (less than 0.03) between populations, with a larger amount of migration from Finland to Karelia than vice versa. Our findings emphasise the role of physical obstacles and territorial behaviour in creating barriers to gene flow between populations in relatively limited geographical areas, even in large-bodied mammalian species with long-distance dispersal capabilities and an apparently continuous population structure.     

Differences in sexual behavior of two distant populations of the funnel-web wolf spider Aglaoctenus lagotis

Generally, sexual repertoire within a species is conserved, but frequencies of occurrence of sexual behavioral acts often vary, and wide geographic distributions may favor these variations. Aglaoctenus lagotis is distributed along South America and belongs to Sosippinae, a subfamily of wolf spiders that builds funnel webs. Previous reports, based on different populations, suggested variations in sexual behavior and life cycle. Our objective was to describe and compare the sexual behavior of two populations of A. lagotis: ‘Southern Uruguay’ (SU) and ‘Central Argentina’ (CA). We carried out intrapopulation trials, in the laboratory, with 15 female–male pair matings. The most representative courtship acts in SU were web-stretching, striding-forward and forelegs-elevating, whereas in CA they were alternate-waving, web-stretching and leg-tapping. Juddering, forelegs-elevating and striding-forward were exclusive for SU, while alternate-waving and simultaneous-waving were exclusive for CA. We also found differences in copulatory characteristics such as frequencies of insertions and ejaculations. We documented body-shaking during copulation for the first time. Some sexual acts were exclusive of each population, while the shared ones differed in pattern and frequencies of occurrence. In addition to variations in sexual periods, these differences may favor divergence processes or an exceptional high level of flexibility in the sexual behavior of A. lagotis.     

Genetic diversity in fragmented populations of the critically endangered spider orchid Caladenia huegelii: implications for conservation

The Orchidaceae is characterised by a diverse range of life histories, reproductive strategies and geographic distribution, reflected in a variety of patterns in the population genetic structure of different species. In this study, the genetic diversity and structure was assessed within and among remnant populations of the critically endangered sexually deceptive orchid, Caladenia huegelii. This species has experienced severe recent habitat loss in a landscape marked by ancient patterns of population fragmentation within the Southwest Australian Floristic Region, a global biodiversity hotspot. Using seven polymorphic microsatellite loci, high levels of within-population diversity (mean alleles/locus = 6.73; mean H _E = 0.690), weak genetic structuring among 13 remnant populations (F _ST = 0.047) and a consistent deficit of heterozygotes from Hardy–Weinberg expectation were found across all populations (mean F _IS = 0.22). Positive inbreeding coefficients are most likely due to Wahlund effects and/or inbreeding effects from highly correlated paternity and typically low fruit set. Indirect estimates of gene flow (Nm = 5.09 using F _ST; Nm = 3.12 using the private alleles method) among populations reflects a historical capacity for gene flow through long distance pollen dispersal by sexually deceived wasp pollinators and/or long range dispersal of dust-like orchid seed. However, current levels of gene flow may be impacted by habitat destruction, fragmentation and reduced population size. A genetically divergent population was identified, which should be a high priority for conservation managers. Very weak genetic differentiation indicates that the movement and mixing of seeds from different populations for reintroduction programs should result in minimal negative genetic effects.     

Estimates of gene flow among neighbouring populations of brown trout

Between-population gene flow was estimated in neighbouring freshwater and anadromous Salmo trutta populations from Asturias, Northern Spain. Populations from the same drainage showed a high mean level of gene flow. Gene flow was also found between populations from different drainages and was negatively related to the distance between river mouths. The strength of the homing orientation of migratory individuals (sea trout) is discussed.     

Energetic costs of size and sexual signalling in a wolf spider

A prerequisite for honest handicaps is that there are significant condition-dependent costs in the expression of sexual traits. In the wolf spider Hygrolycosa rubrofasciata (Ohlert), sexual signalling (drumming) is costly in terms of increased mortality. Here we investigated whether this mortality may be caused by increased energy expenditure. During sexual signalling, metabolic rate was 22 times higher than at rest and four times higher than when males were actively moving. Metabolic rate per unit mass was positively related to absolute body mass during sexual signalling but not during other activities. This positive relationship is novel to any studies of metabolic rates. Indeed, it seems that the largest males can drum only 12 times per minute before reaching the maximum sustainable metabolic rate, whereas the smallest males may drum up to 39 times per minute. However, there is no relationship between body mass and drumming rate, indicating that larger males are able to compensate for the higher cost of drumming. There was a quadratic relationship between relative abdomen mass and overall body mass, which may provide a partial explanation for the increased energy expenditure of largest males while drumming. Altogether, our results indicate that sexual signalling is highly energetically demanding, which may be the main reason for the honesty of signalling in this species. In addition, the energetic costs are surprisingly strongly size dependent, which may compensate any disadvantage of small male size.     

Immigration rates in fragmented landscapes--empirical evidence for the importance of habitat amount for species persistence

Background

The total amount of native vegetation is an important property of fragmented landscapes and is known to exert a strong influence on population and metapopulation dynamics. As the relationship between habitat loss and local patch and gap characteristics is strongly non-linear, theoretical models predict that immigration rates should decrease dramatically at low levels of remaining native vegetation cover, leading to patch-area effects and the existence of species extinction thresholds across fragmented landscapes with different proportions of remaining native vegetation. Although empirical patterns of species distribution and richness give support to these models, direct measurements of immigration rates across fragmented landscapes are still lacking.

Methodology/Principal Findings

Using the Brazilian Atlantic forest marsupial Gray Slender Mouse Opossum (Marmosops incanus) as a model species and estimating demographic parameters of populations in patches situated in three landscapes differing in the total amount of remaining forest, we tested the hypotheses that patch-area effects on population density are apparent only at intermediate levels of forest cover, and that immigration rates into forest patches are defined primarily by landscape context surrounding patches. As expected, we observed a positive patch-area effect on M. incanus density only within the landscape with intermediate forest cover. Density was independent of patch size in the most forested landscape and the species was absent from the most deforested landscape. Specifically, the mean estimated numbers of immigrants into small patches were lower in the landscape with intermediate forest cover compared to the most forested landscape.

Conclusions/Significance

Our results reveal the crucial importance of the total amount of remaining native vegetation for species persistence in fragmented landscapes, and specifically as to the role of variable immigration rates in providing the underlying mechanism that drives both patch-area effects and species extinction thresholds.     

The influence of anthropogenic edge effects on primate populations and their habitat in a fragmented rainforest in Costa Rica

When a forest is fragmented, this increases the amount of forest edge relative to the interior. Edge effects can lead to loss of animal and plant species and decreased plant biomass near forest edges. We examined the influence of an anthropogenic forest edge comprising cattle pasture, coconut plantations, and human settlement on the mantled howler (Alouatta palliata), white-faced capuchin (Cebus capucinus), Central American spider monkey (Ateles geoffroyi), and plant populations at La Suerte Biological Research Station (LSBRS), Costa Rica. We predicted that there would be lower monkey encounter rate, mean tree species richness, and diameter at breast height (DBH) in forest edge versus interior, and that monkeys would show species-specific responses to edge based on diet, body size, and canopy height preferences. Specifically, we predicted that howler monkeys would show positive or neutral edge effects due to their flexible folivorous diet, large body size, and preference for high canopy, capuchins would show positive edge effects due to their diverse diet, small body size, and preference for low to middle canopy, and spider monkeys would show negative edge effects due their reliance on ripe fruit, large body size, and preference for high upper canopy. We conducted population and vegetation surveys along edge and interior transects at LSBRS. Contrary to predictions, total monkey encounter rate did not vary between the forest edge and forest interior. Furthermore, all three species showed neutral edge effects with no significant differences in encounter rate between forest edge and interior. Interior transects had significantly higher mean tree species richness than edge transects, and interior trees had greater DBH than edge trees, although this difference was not significant. These results suggest that forest edges negatively impact plant populations at La Suerte but that the monkeys are able to withstand these differences in vegetation.     

Seascape analysis reveals regional gene flow patterns among populations of a marine planktonic diatom

We investigated the gene flow of the common marine diatom, Skeletonema marinoi, in Scandinavian waters and tested the null hypothesis of panmixia. Sediment samples were collected from the Danish Straits, Kattegat and Skagerrak. Individual strains were established from germinated resting stages. A total of 350 individuals were genotyped by eight microsatellite markers. Conventional F-statistics showed significant differentiation between the samples. We therefore investigated whether the genetic structure could be explained using genetic models based on isolation by distance (IBD) or by oceanographic connectivity. Patterns of oceanographic circulation are seasonally dependent and therefore we estimated how well local oceanographic connectivity explains gene flow month by month. We found no significant relationship between genetic differentiation and geographical distance. Instead, the genetic structure of this dominant marine primary producer is best explained by local oceanographic connectivity promoting gene flow in a primarily south to north direction throughout the year. Oceanographic data were consistent with the significant F_ST values between several pairs of samples. Because even a small amount of genetic exchange prevents the accumulation of genetic differences in F-statistics, we hypothesize that local retention at each sample site, possibly as resting stages, is an important component in explaining the observed genetic structure.     

Flexibility in the multi-modal courtship of a wolf spider, Schizocosa ocreata

Male Schizocosa ocreata wolf spiders court females with synchronous visual and seismic displays. We tested whether male S. ocreata modify their courtship in relation to light environment, and associated utility of the visual components. Males were generally more active and more likely to perform the major courtship element (jerky tapping) when in the light. One courtship element (arching) was only observed in the light while another (vertical leg-extend) was only observed in the dark. Courtship in the dark retained visual components, suggesting spiders cannot disengage these components of multi-modal display even when superfluous. Once initiated, there was no evidence that performance rate or time spent in each courtship element differed in the light and in the dark.     

Repeated sampling detects gene flow in a flightless ground beetle in a fragmented landscape

Secondary clines level down in the course of time if the gene flow is not interrupted. Temporally repeated sampling of populations in a cline allows the investigation not only of its occurrence but also of the estimation of the amount of ongoing gene flow. We reinvestigated an allozyme gradient in Carabus auronitens populations in the Westphalian Lowlands (northwestern Germany) 15 to 20 years after it had originally been recorded. A total of 977 individuals of this flightless woodland species from 29 sample sites were genotyped at the diallelic Est-1 locus in 2005-2006 and compared to former findings, collected in 1985-1994 from the same populations. Both data sets showed clinal variation. Pairwise differences between the samples of both data sets indicated significant decrease in the steepness of the cline during the past 15 to 20 years. The estimated average gene flow per generation is 0.6% of each beetle population. Ongoing gene flow in the flightless ground beetle C. auronitens led to a less pronounced cline despite a stable degree of fragmentation (and connectivity) of the landscape. Migration and gene flow were obviously enabled by the numerous hedgerows. The corridors are seen to be a prerequisite for migration between populations and for possible future range shifts of forest insect species.