Divergence genetics analysis reveals historical population genetic processes leading to contrasting phylogeographic patterns in co-distributed species

Coalescent samplers are computational time machines for inferring the historical demographic genetic processes that have given rise to observable patterns of spatial genetic variation among contemporary populations. We have used traditional characterizations of population structure and coalescent‐based inferences about demographic processes to reconstruct the population histories of two co‐distributed marine species, the frilled dog whelk, Nucella lamellosa, and the bat star, Patiria miniata. Analyses of population structure were consistent with previous work in both species except that additional samples of N. lamellosa showed a larger regional genetic break on Vancouver Island (VI) rather than between the southern Alexander Archipelago as in P. miniata. Our understanding of the causes, rather than just the patterns, of spatial genetic variation was dramatically improved by coalescent analyses that emphasized variation in population divergence times. Overall, gene flow was greater in bat stars (planktonic development) than snails (benthic development) but spatially homogeneous within species. In both species, these large phylogeographic breaks corresponded to relatively ancient divergence times between populations rather than regionally restricted gene flow. Although only N. lamellosa shows a large break on VI, population separation times on VI are congruent between species, suggesting a similar response to late Pleistocene ice sheet expansion. The absence of a phylogeographic break in P. miniata on VI can be attributed to greater gene flow and larger effective population size in this species. Such insights put the relative significance of gene flow into a more comprehensive historical biogeographic context and have important implications for conservation and landscape genetic studies that emphasize the role of contemporary gene flow and connectivity in shaping patterns of population differentiation.     

The extent and costs of reproductive interference among four species of true bug

Reproductive interference arises when individuals of one species engage in reproductive activities with individuals of another, leading to fitness costs in one or both species. Reproductive interference (RI) therefore has two components. First, there must be mis-directed mating interactions. Second, there must be costs associated with these mis-directed interactions. Here we consider RI between four species of true bug in the family Lygaeidae, focusing in particular on the fitness consequences to Lygaeus equestris. The species we consider vary in their relationships with each other, including species in the same or different genus, and with or without natural overlap in their geographic ranges. First we show that inter-specific mating interactions, although not a certain outcome, are common enough to perhaps influence mating behaviour in these species (arising in up to 10 % of inter-specific pairings). Second, we show that reproductive interference can seriously reduce female fitness in L. equestris. Importantly, different species impose different costs of RI on L. equestris, with interactions with male Spilostethus pandurus inflicting fitness costs of similar magnitude to the costs of mating with con-specifics. On the other hand, mating interactions with male Oncopeltus fasciatus appear to have no effect on female fitness. In a follow-up experiment, when we allowed competition amongst just females of S. pandurus and L. equestris, the fitness of the latter was not reduced, arguing more strongly for the role of reproductive interference. However, in our final experiments under mass mating conditions with extended ecological interactions (including scope for competition for resources and cannibalism), the costs of RI were less apparent. Our data therefore suggest that the costs of RI will be context-specific and may act in concert with, or be swamped by, other ecological effects. We suggest that comparative studies of this sort that both mimic naturally occurring reproductive interference events, and also artificially generate new ones, will be necessary if we are to better understand the ecological and evolutionary significance of reproductive interference.     

Contrasting genetic structure in two co-distributed species of old world fruit bat

The fulvous fruit bat (Rousettus leschenaulti) and the greater short-nosed fruit bat (Cynopterus sphinx) are two abundant and widely co-distributed Old World fruit bats in Southeast and East Asia. The former species forms large colonies in caves while the latter roots in small groups in trees. To test whether these differences in social organization and roosting ecology are associated with contrasting patterns of gene flow, we used mtDNA and nuclear loci to characterize population genetic subdivision and phylogeographic histories in both species sampled from China, Vietnam and India. Our analyses from R. leschenaulti using both types of marker revealed little evidence of genetic structure across the study region. On the other hand, C. sphinx showed significant genetic mtDNA differentiation between the samples from India compared with China and Vietnam, as well as greater structuring of microsatellite genotypes within China. Demographic analyses indicated signatures of past rapid population expansion in both taxa, with more recent demographic growth in C. sphinx. Therefore, the relative genetic homogeneity in R. leschenaulti is unlikely to reflect past events. Instead we suggest that the absence of substructure in R. leschenaulti is a consequence of higher levels of gene flow among colonies, and that greater vagility in this species is an adaptation associated with cave roosting.     

The effects of subdivision on the genetic divergence of populations and species

Abstract. An island model of migration is used to study the effects of subdivision within populations and species on sample genealogies and on between-population or between-species measures of genetic variation. The model assumes that the number of demes within each population or species is large. When populations (or species), connected either by gene flow or historical association, are themselves subdivided into demes, changes in the migration rate among demes alter both the structure of genealogies and the time scale of the coalescent process. The time scale of the coalescent is related to the effective size of the population, which depends on the migration rate among demes. When the migration rate among demes within populations is low, isolation (or speciation) events seem more recent and migration rates among populations seem higher because the effective size of each population is increased. This affects the probability of reciprocal monophyly of two samples, the chance that a gene tree of a sample matches the species tree, and relative likelihoods of different types of polymorphic sites. It can also have a profound effect on the estimation of divergence times.     

Testing for population subdivision and association in four case-control studies

Population structure has been presumed to cause many of the unreplicated disease-marker associations reported in the literature, yet few actual case-control studies have been evaluated for the presence of structure. Here, we examine four moderate case-control samples, comprising 3,472 individuals, to determine if detectable population subdivision is present. The four population samples include: 500 U.S. whites and 236 African Americans with hypertension; and 500 U.S. whites and 500 Polish whites with type 2 diabetes, all with matched control subjects. Both diabetes populations were typed for the PPARg Pro12Ala polymorphism, to replicate this well-supported association (Altshuler et al. 2000). In each of the four samples, we tested for structure, using the sum of the case-control allele frequency chi(2) statistics for 9 STR and 35 SNP markers (Pritchard and Rosenberg 1999). We found weak evidence for population structure in the African American sample only, but further refinement of the sample, to include only individuals with U.S.-born parents and grandparents, eliminated the stratification. Our examples provide insight into the factors affecting the replication of association studies and suggest that carefully matched, moderate-sized case-control samples in cosmopolitan U.S. and European populations are unlikely to contain levels of structure that would result in significantly inflated numbers of false-positive associations. We explore the role that extreme differences in power among studies, due to sample size and risk-allele frequency differences, may play in the replication problem.     

Islands increase genetic subdivision and disrupt patterns of connectivity of intertidal snails in a complex archipelago

The view that marine species with planktonic dispersal have highly connected, demographically open populations is giving way to recognition that populations may often be largely self-recruiting, or demographically closed. This raises the question of what local conditions might favor isolation of populations. To test the importance of islands for local isolation in species with planktonic larvae, we examined allozyme variation among 35 populations of the intertidal snail Austrocochlea constricta in the Houtman Abrolhos Islands, Western Australia, spanning 60 km. Heterogeneity of allozyme frequencies among populations was high, with average F(ST) of 0.237, indicating highly localized populations. Increased subdivision was associated with islands at different scales: between island groups, separated by deep water gaps, and between disconnected sets of islands within groups. At short distances, up to two km, subdivision increased fivefold between islands compared with that between populations on the same island. Along 11 km of continuous, sheltered shore, there was isolation by distance but among a linear series of islands over similar distance, there was greater subdivision at short distances but no association with distance. These patterns had been seen previously in the direct-developing snail Bembicium vittatum, but its finding in A. constricta confirms for a planktonic disperser the importance of this complex archipelago for both retention of locally produced larvae and disruption of patterns of connectivity. Taken together, these results indicate that islands can increase both the "open" and the "closed" components of recruitment and that applicable models of genetic connectivity depend substantially on local conditions.     

Alfred R. Wallace's enduring influence on biogeographical studies of the Indo-Australian archipelago

To mark A.R. Wallace's 200th birthday, we review the direct and indirect contributions he made to our understanding of the Indo-Australian Archipelago's biogeography. He is widely known for his field research (1854–1862) and his 1863 boundary line separating the Oriental and Australasian faunal realms (between Bali and Lombok, Borneo and Sulawesi, and the Philippines and the Moluccas). Notably, though, he never accepted Huxley's ‘Wallace Line’ proposal (1868), whose northern part runs between the main Philippine islands and the Palawan Group to the west. Furthermore, in 1910, which was 3 years prior to his demise, he transferred Sulawesi's fauna to the Oriental realm. In 1924, Merrill introduced the ‘Wallacea’ transition zone. Although the label is today widely used to denote a sub-region within the Indo-Australian Archipelago between Wallace's 1863 line and Lydekker's 1896 line (first presented by Darlington in 1957), the western boundary was originally based on Huxley's line, and thus included the Philippine islands minus the Palawan group. Most biogeographers appear to be unaware of Merrill and his intention. Finally, recent attempts to define the faunal break have not led to a consensus view, despite the huge increase in primary data plus the application of modern analytical techniques. This reflects the complexities and diversity of the region's faunal distribution patterns, plus the differences in the ways that researchers choose to process their data.     

Emergence activity at hibernacula differs among four bat species affected by white‐nose syndrome

Prior to the introduction of white‐nose syndrome (WNS) to North America, temperate bats were thought to remain within hibernacula throughout most of the winter. However, recent research has shown that bats in the southeastern United States emerge regularly from hibernation and are active on the landscape, regardless of their WNS status. The relationship between winter activity and susceptibility to WNS has yet to be explored but warrants attention, as it may enable managers to implement targeted management for WNS‐affected species. We investigated this relationship by implanting 1346 passive integrated transponder (PIT) tags in four species that vary in their susceptibility to WNS. Based on PIT‐tag detections, three species entered hibernation from late October to early November. Bats were active at hibernacula entrances on days when midpoint temperatures ranged from −1.94 to 22.78°C (mean midpoint temperature = 8.70 ± 0.33°C). Eastern small‐footed bats (Myotis leibii), a species with low susceptibility to WNS, were active throughout winter, with a significant decrease in activity in mid‐hibernation (December 16 to February 15). Tricolored bats (Perimyotis subflavus), a species that is highly susceptible to WNS, exhibited an increase in activity beginning in mid‐hibernation and extending through late hibernation (February 16 to March 31). Indiana bats (M. sodalis), a species determined to have a medium–high susceptibility to WNS, remained on the landscape into early hibernation (November 1 to December 15), after which we did not record any again until the latter portion of mid‐hibernation. Finally, gray bats (M. grisescens), another species with low susceptibility to WNS, maintained low but regular levels of activity throughout winter. Given these results, we determined that emergence activity from hibernacula during winter is highly variable among bat species and our data will assist wildlife managers to make informed decisions regarding the timing of implementation of species‐specific conservation actions.     

Population genetics of four heavily exploited shark species around the Arabian Peninsula

The northwestern Indian Ocean harbors a number of larger marine vertebrate taxa that warrant the investigation of genetic population structure given remarkable spatial heterogeneity in biological characteristics such as distribution, behavior, and morphology. Here, we investigate the genetic population structure of four commercially exploited shark species with different biological characteristics (Carcharhinus limbatus, Carcharhinus sorrah, Rhizoprionodon acutus, and Sphyrna lewini) between the Red Sea and all other water bodies surrounding the Arabian Peninsula. To assess intraspecific patterns of connectivity, we constructed statistical parsimony networks among haplotypes and estimated (1) population structure; and (2) time of most recent population expansion, based on mitochondrial control region DNA and a total of 20 microsatellites. Our analysis indicates that, even in smaller, less vagile shark species, there are no contemporary barriers to gene flow across the study region, while historical events, for example, Pleistocene glacial cycles, may have affected connectivity in C. sorrah and R. acutus. A parsimony network analysis provided evidence that Arabian S. lewini may represent a population segment that is distinct from other known stocks in the Indian Ocean, raising a new layer of conservation concern. Our results call for urgent regional cooperation to ensure the sustainable exploitation of sharks in the Arabian region.     

The coalescent in an island model of population subdivision with variation among demes

A simple genealogical structure is found for a general finite island model of population subdivision. The model allows for variation in the sizes of demes, in contributions to the migrant pool, and in the fraction of each deme that is replaced by migrants every generation. The ancestry of a sample of non-recombining DNA sequences has a simple structure when the sample size is much smaller than the total number of demes in the population. This allows an expression for the probability distribution of the number of segregating sites in the sample to be derived under the infinite-sites mutation model. It also yields easily computed estimators of the migration parameter for each deme in a multi-deme sample. The genealogical process is such that the lineages ancestral to the sample tend to accumulate in demes with low migration rates and/or which contribute disproportionately to the migrant pool. In addition, common ancestor or coalescent events tend to occur in demes of small size. This provides a framework for understanding the determinants of the effective size of the population, and leads to an expression for the probability that the root of a genealogy occurs in a particular geographic region, or among a particular set of demes.     

Plant species as indicators of the extent of desertification in four sandy rangelands

We examined the distribution of plants in sandy rangelands with different degrees of desertification in (i) Horqin and Mu Us sandy lands in north China, (ii) Darfur district in north‐west Sudan and (iii) southern Tunisia. The severity of desertification in these areas was classified as light, moderate, severe or extreme. The following vegetation changes were observed with increasing severity of desertification: a decrease in the number of plant species, an increase in drought‐tolerant plants, a decrease in the proportion of palatable grasses and the occurrence of some species in only one category of desertification, whereas other species occurred in several categories. Plant species with unique niche requirements were identified and recommended as indicators of the degree of desertification for particular areas. We discuss the characteristics of species in areas with severe desertification and the method of using plant species as indicators of the extent of desertification.     

Concordant genetic breaks, identified by combining clustering and tessellation methods, in two co-distributed alpine plant species

Natural genetic breaks may indicate limitations to gene flow or the presence of contact zones of previously isolated populations. Molecular evidence suggests that genetic breaks have aggregated in distinct geographical areas. We propose a new application of well-established statistical methods for analysing multilocus genetic data to identify intraspecific genetic breaks. The methodological approach combines Bayesian clustering with a spatially explicit maximum-difference algorithm to visualize and quantify breaks between clusters. We used amplified fragment length polymorphism data of two co-distributed, silicicolous alpine plant species, Geum montanum and Geum reptans , exhaustively sampled on a consistent, regular grid over their entire range of the European Alps and the Carpathians. We found a distinct and highly similar allocation of genetic breaks in both species. The pattern of breaks did not conform to scenarios of glacial refugial survival, alternatively in peripheral refugia or on nunataks, as expected because of the species' ecologies (late-successional low alpine vs. early-successional high alpine). Our findings rather substantiated the postulate of a general pattern of genetic breaks in alpine plants and corresponded well with biogeographical regions formerly described. Our approach could serve as a tool not only for landscape genetics and comparative phylogeography, but also for floristics or faunistics to compare biogeographic with phylogeographic breaks.     

Typing of four genetic loci discriminates among closely related species of New World Leishmania

All New World Leishmania species can cause cutaneous lesions, while only Leishmania (Viannia) braziliensis has been associated with mucosal metastases. Multilocus enzyme electrophoresis (MLEE) is the optimal standard for species identification but is slow and costly. New methods for species identification are needed to ensure proper identification and therapy. The coding regions of four metabolic enzyme markers in the MLEE typing method: mannose phosphate isomerase (MPI), malate dehydrogenase (MDH), glucose-6-phosphate isomerase (GPI), and 6-phosphogluconate dehydrogenase (6PGD), were analysed from seven species of New World Leishmania isolated from patients with either cutaneous or mucosal lesions to identify specific genetic polymorphisms responsible for the phenotypic variations observed in the MLEE typing scheme. We identified species-specific polymorphisms and determined that a combination of sequencing of the mpi and 6pgd genes was sufficient to differentiate among seven closely related species of New World Leishmania and among isolates of L. braziliensis shown previously to have atypical MLEE patterns. When DNA isolated from 10 cutaneous lesion biopsies were evaluated, the sequence typing method was 100% concordant with the published MLEE/monoclonal antibody identification methods. The identification of species-specific polymorphisms can be used to design a DNA-based test with greater discriminatory power that requires shorter identification times. When the causative agent of the disease is L. braziliensis, this method ensures correct species identification, even when the agent is a genetic variant. Proper identification could facilitate adequate treatment, preventing the onset of the disfiguring mucosal form of the disease.     

Correlates of dispersal extent predict the degree of population genetic structuring in bats

Dispersal is essential for maintaining demographic and genetic connectivity. For bats, correlates of dispersal extent such as morphology and movement dynamics are reported as having an influence on population genetic structure although these traits exhibit co-variance which has not been previously examined. We used a principal components framework with phylogenetically independent contrasts to compare five dispersal extent predictors (wing loading, aspect ratio, geographic range size, migratory status and median latitude) with population genetic structure among bats. We found that high wing loading values and migration negatively correlate with genetic structure after accounting for co-variance. These findings suggest that bats that can achieve higher flight speeds and migrate seasonally have higher gene flow and resultant genetic connectivity relative to bats that fly slower and do not migrate. These results represent a step towards understanding factors that shaped the genetic structure of bat populations.     

Spatial extent of analysis influences observed patterns of population genetic structure in a widespread darter species (Percidae)

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Loss of genetic variability in social spiders: genetic and phylogenetic consequences of population subdivision and inbreeding

The consequences of population subdivision and inbreeding have been studied in many organisms, particularly in plants. However, most studies focus on the short‐term consequences, such as inbreeding depression. To investigate the consequences of both population fragmentation and inbreeding for genetic variability in the longer term, we here make use of a natural inbreeding experiment in spiders, where sociality and accompanying population subdivision and inbreeding have evolved repeatedly. We use mitochondrial and nuclear data to infer phylogenetic relationships among 170 individuals of Anelosimus spiders representing 23 species. We then compare relative mitochondrial and nuclear genetic variability of the inbred social species and their outbred relatives. We focus on four independently derived social species and four subsocial species, including two outbred–inbred sister species pairs. We find that social species have 50% reduced mitochondrial sequence divergence. As inbreeding is not expected to reduce genetic variability in the maternally inherited mitochondrial genome, this suggests the loss of variation due to strong population subdivision, founder effects, small effective population sizes (colonies as individuals) and lineage turnover. Social species have < 10% of the nuclear genetic variability of the outbred species, also suggesting the loss of genetic variability through founder effects and/or inbreeding. Inbred sociality hence may result in reduction in variability through various processes. Sociality in most Anelosimus species probably arose relatively recently (0.1–2 mya), with even the oldest social lineages having failed to diversify. This is consistent with the hypothesis that inbred spider sociality represents an evolutionary dead end. Heterosis underlies a species potential to respond to environmental change and/or disease. Inbreeding and loss of genetic variability may thus limit diversification in social Anelosimus lineages and similarly pose a threat to many wild populations subject to habitat fragmentation or reduced population sizes.     

Contemporary population structure and post‐glacial genetic demography in a migratory marine species,the blacknose shark,Carcharhinus acronotus

Patterns of population structure and historical genetic demography of blacknose sharks in the western North Atlantic Ocean were assessed using variation in nuclear‐encoded microsatellites and sequences of mitochondrial (mt)DNA. Significant heterogeneity and/or inferred barriers to gene flow, based on microsatellites and/or mtDNA, revealed the occurrence of five genetic populations localized to five geographic regions: the southeastern U.S Atlantic coast, the eastern Gulf of Mexico, the western Gulf of Mexico, Bay of Campeche in the southern Gulf of Mexico and the Bahamas. Pairwise estimates of genetic divergence between sharks in the Bahamas and those in all other localities were more than an order of magnitude higher than between pairwise comparisons involving the other localities. Demographic modelling indicated that sharks in all five regions diverged after the last glacial maximum and, except for the Bahamas, experienced post‐glacial, population expansion. The patterns of genetic variation also suggest that the southern Gulf of Mexico may have served as a glacial refuge and source for the expansion. Results of the study demonstrate that barriers to gene flow and historical genetic demography contributed to contemporary patterns of population structure in a coastal migratory species living in an otherwise continuous marine habitat. The results also indicate that for many marine species, failure to properly characterize barriers in terms of levels of contemporary gene flow could in part be due to inferences based solely on equilibrium assumptions. This could lead to erroneous conclusions regarding levels of connectivity in species of conservation concern.     

Global population genetic dynamics of a highly migratory,apex predator shark

Knowledge of genetic connectivity dynamics in the world's large‐bodied, highly migratory, apex predator sharks across their global ranges is limited. One such species, the tiger shark (Galeocerdo cuvier), occurs worldwide in warm temperate and tropical waters, uses remarkably diverse habitats (nearshore to pelagic) and possesses a generalist diet that can structure marine ecosystems through top‐down processes. We investigated the phylogeography and the global population structure of this exploited, phylogenetically enigmatic shark by using 10 nuclear microsatellites (n = 380) and sequences from the mitochondrial control region (CR, n = 340) and cytochrome oxidase I gene (n = 100). All three marker classes showed the genetic differentiation between tiger sharks from the western Atlantic and Indo‐Pacific ocean basins (microsatellite F_ST > 0.129; CR Φ_ST > 0.497), the presence of North vs. southwestern Atlantic differentiation and the isolation of tiger sharks sampled from Hawaii from other surveyed locations. Furthermore, mitochondrial DNA revealed high levels of intraocean basin matrilineal population structure, suggesting female philopatry and sex‐biased gene flow. Coalescent‐ and genetic distance‐based estimates of divergence from CR sequences were largely congruent (d_corr = 0.0015–0.0050), indicating a separation of Indo‐Pacific and western Atlantic tiger sharks <1 million years ago. Mitochondrial haplotype relationships suggested that the western South Atlantic Ocean was likely a historical connection for interocean basin linkages via the dispersal around South Africa. Together, the results reveal unexpectedly high levels of population structure in a highly migratory, behaviourally generalist, cosmopolitan ocean predator, calling for management and conservation on smaller‐than‐anticipated spatial scales.     

Modeling population genetic data in autotetraploid species

Allozyme and PCR-based molecular markers have been widely used to investigate genetic diversity and population genetic structure in autotetraploid species. However, an empirical but inaccurate approach was often used to infer marker genotype from the pattern and intensity of gel bands. Obviously, this introduces serious errors in prediction of the marker genotypes and severely biases the data analysis. This article developed a theoretical model to characterize genetic segregation of alleles at genetic marker loci in autotetraploid populations and a novel likelihood-based method to estimate the model parameters. The model properly accounts for segregation complexities due to multiple alleles and double reduction at autotetrasomic loci in natural populations, and the method takes appropriate account of incomplete marker phenotype information with respect to genotype due to multiple-dosage allele segregation at marker loci in tetraploids. The theoretical analyses were validated by making use of a computer simulation study and their utility is demonstrated by analyzing microsatellite marker data collected from two populations of sycamore maple (Acer pseudoplatanus L.), an economically important autotetraploid tree species. Numerical analyses based on simulation data indicate that the model parameters can be adequately estimated and double reduction is detected with good power using reasonable sample size.