Bioclimatic regions influence genetic structure of four Jordanian Stipa species

Strong environmental gradients can affect the genetic structure of plant populations, but little is known as to whether closely related species respond similarly or idiosyncratically to ecogeographic variation. We analysed the extent to which gradients in temperature and rainfall shape the genetic structure of four Stipa species in four bioclimatic regions in Jordan. Genetic diversity, differentiation and structure of Stipa species were investigated using amplified fragment length polymorphism (AFLP) molecular markers. For each of the four study species, we sampled 120 individuals from ten populations situated in distinct bioclimatic regions and assessed the degree of genetic diversity and genetic differentiation within and among populations. The widespread ruderals Stipa capensis and S. parviflora had higher genetic diversity than the geographically restricted semi‐desert species S. arabica and S. lagascae. In three of the four species, genetic diversity strongly decreased with precipitation, while genetic diversity increased with temperature in S. capensis. Most genetic diversity resided among populations in the semi‐desert species (Φ_ST = 0.572/0.595 in S. arabica/lagascae) but within populations in the ruderal species (Φ_ST = 0.355/0.387 S. capensis/parviflora). Principal coordinate analysis ( PCoA) and STRUCTURE analysis showed that Stipa populations of all species clustered ecogeographically. A genome scan revealed that divergent selection at particular AFLP loci contributed to genetic differentiation. Irrespective of their different life histories, Stipa species responded similarly to the bioclimatic gradient in Jordan. We conclude that, in addition to predominant random processes, steep climatic gradients might shape the genetic structure of plant populations.     

Genetic structure is correlated with phenotypic divergence rather than geographic isolation in the highly polymorphic strawberry poison‐dart frog

Phenotypic and genetic divergence can be influenced by a variety of factors, including sexual and natural selection, genetic drift and geographic isolation. Investigating the roles of these factors in natural systems can provide insight into the relative influences of allopatric and ecological modes of biological diversification in nature. The strawberry poison frog, Dendrobates pumilio, presents an excellent opportunity for this kind of research, displaying a diverse array of colour morphs and inhabiting a heterogeneous landscape that includes oceanic islands, fragmented rainforest patches and wide expanses of suitable habitat. In this study, we use 15 highly polymorphic microsatellite loci to estimate population structure and gene flow among populations from across the range of D. pumilio and a causal modelling framework to statistically test 12 hypotheses regarding the geographic and phenotypic variables that explain genetic differentiation within this system. Our results demonstrate that the genetic distance between populations is most strongly associated with differences in dorsal coloration. Previous experimental studies have shown that phenotypic differences can result in sexual and natural selection against non‐native phenotypes, and our results now show that these forces lead to genetic isolation between different colour morphs in the wild, presenting a potential case of incipient speciation through selection.     

Testing evolutionary hypotheses for phenotypic divergence using landscape genetics

Understanding the evolutionary causes of phenotypic variation among populations has long been a central theme in evolutionary biology. Several factors can influence phenotypic divergence, including geographic isolation, genetic drift, divergent natural or sexual selection, and phenotypic plasticity. But the relative importance of these factors in generating phenotypic divergence in nature is still a tantalizing and unresolved problem in evolutionary biology. The origin and maintenance of phenotypic divergence is also at the root of many ongoing debates in evolutionary biology, such as the extent to which gene flow constrains adaptive divergence ( Garant et al. 2007 ) and the relative importance of genetic drift, natural selection, and sexual selection in initiating reproductive isolation and speciation ( Coyne & Orr 2004 ). In this issue, Wang & Summers (2010) test the causes of one of the most fantastic examples of phenotypic divergence in nature: colour pattern divergence among populations of the strawberry poison frog (Dendrobates pumilio) in Panama and Costa Rica ( Fig. 1 ). This study provides a beautiful example of the use of the emerging field of landscape genetics to differentiate among hypotheses for phenotypic divergence. Using landscape genetic analyses, Wang & Summers were able to reject the hypotheses that colour pattern divergence is due to isolation‐by‐distance (IBD) or landscape resistance. Instead, the hypothesis left standing is that colour divergence is due to divergent selection, in turn driving reproductive isolation among populations with different colour morphs. More generally, this study provides a wonderful example of how the emerging field of landscape genetics, which has primarily been applied to questions in conservation and ecology, now plays an essential role in evolutionary research.

Figure 1 Open in figure viewer PowerPoint Divergent colour morphs observed among populations of the strawberry poison frog, Dendrobates pumilio. Frogs are from San Cristobal (upper left), Cerro Brujo (upper right), Bastimentos (lower right), and Agua (lower left).     

Hybridization promotes color polymorphism in the aposematic harlequin poison frog,Oophaga histrionica

Whether hybridization can be a mechanism that drives phenotypic diversity is a widely debated topic in evolutionary biology. In poison frogs (Dendrobatidae), assortative mating has been invoked to explain how new color morphs persist despite the expected homogenizing effects of natural selection. Here, we tested the complementary hypothesis that new morphs arise through hybridization between different color morphs. Specifically, we (1) reconstructed the phylogenetic relationships among the studied populations of a dart‐poison frog to provide an evolutionary framework, (2) tested whether microsatellite allele frequencies of one putative hybrid population of the polymorphic frog O. histrionica are intermediate between O. histrionica and O. lehmanni, and (3) conducted mate‐choice experiments to test whether putatively intermediate females prefer homotypic males over males from the other two populations. Our findings are compatible with a hybrid origin for the new morph and emphasize the possibility of hybridization as a mechanism generating variation in polymorphic species. Moreover, because coloration in poison frogs is aposematic and should be heavily constrained, our findings suggest that hybridization can produce phenotypic novelty even in systems where phenotypes are subject to strong stabilizing selection.     

Genetic differentiation between the ant Myrmica rubra and its microgynous social parasite

Hymenopteran inquiline species have been proposed to originate by sympatric speciation through intraspecific social parasitism. One such parasite, Myrmica microrubra, was recently synonymized with its Myrmica rubra host, because comparisons across Europe indicated insufficient genetic differentiation. Here, we use microsatellite markers to study genetic differentiation more precisely in a sample of Finnish M. rubra and its inquilines collected at two localities, supplemented with mitochondrial DNA sequences. The parasite had much lower genetic variation than the host at three of the four loci studied. Genetic differentiation between the host populations was moderate (F _ST = 0.089), whereas the parasite populations were more strongly subdivided (F _ST = 0.440). The host and parasite were highly genetically differentiated both across populations (F _ST = 0.346) and in strict sympatry (0.327, 0.364), a result that remained robust both in a haplotype network and in PCA ordination. Individual assignments of genotypes indicated that gene flow between sympatric host and inquiline populations is reduced by about an order of magnitude relative to the gene flow within the morphs. Our results suggest that the parasitic morph of M. rubra may be an incipient species, but it remains unclear to what extent the observed genetic differentiation between host and inquiline is due to possible assortative mating and selection against hybrids or to recurrent bottlenecking and genetic drift. We conclude that an explicitly functional species concept would be unambiguous in treating this inquiline as a full species, as it begets its own kind and maintains its integrity in spite of occasional interbreeding with the host.     

Evidence for selection on coloration in a Panamanian poison frog: a coalescent‐based approach

Aim The strawberry poison frog, Oophaga pumilio, has undergone a remarkable radiation of colour morphs in the Bocas del Toro archipelago in Panama. This species shows extreme variation in colour and pattern between populations that have been geographically isolated for < 10,000 years. While previous research has suggested the involvement of divergent selection, to date no quantitative test has examined this hypothesis. Location Bocas del Toro archipelago, Panama. Methods We use a combination of population genetics, phylogeography and phenotypic analyses to test for divergent selection in coloration in O. pumilio. Tissue samples of 88 individuals from 15 distinct populations were collected. Using these data, we developed a gene tree using the mitochondrial DNA (mtDNA) d‐loop region. Using parameters derived from our mtDNA phylogeny, we predicted the coalescence of a hypothetical nuclear gene underlying coloration. We collected spectral reflectance and body size measurements on 94 individuals from four of the populations and performed a quantitative analysis of phenotypic divergence. Results The mtDNA d‐loop tree revealed considerable polyphyly across populations. Coalescent reconstructions of gene trees within population trees revealed incomplete genotypic sorting among populations. The quantitative analysis of phenotypic divergence revealed complete lineage sorting by colour, but not by body size: populations showed non‐overlapping variation in spectral reflectance measures of body coloration, while variation in body size did not separate populations. Simulations of the coalescent using parameter values derived from our empirical analyses demonstrated that the level of sorting among populations seen in colour cannot reasonably be attributed to drift. Main conclusions These results imply that divergence in colour, but not body size, is occurring at a faster rate than expected under neutral processes. Our study provides the first quantitative support for the claim that strong diversifying selection underlies colour variation in the strawberry poison frog.     

Population genetics of Setaria viridis,a new model system

An extensive survey of the standing genetic variation in natural populations is among the priority steps in developing a species into a model system. In recent years, green foxtail (Setaria viridis), along with its domesticated form foxtail millet (S. italica), has rapidly become a promising new model system for C₄ grasses and bioenergy crops, due to its rapid life cycle, large amount of seed production and small diploid genome, among other characters. However, remarkably little is known about the genetic diversity in natural populations of this species. In this study, we survey the genetic diversity of a worldwide sample of more than 200 S. viridis accessions, using the genotyping‐by‐sequencing technique. Two distinct genetic groups in S. viridis and a third group resembling S. italica were identified, with considerable admixture among the three groups. We find the genetic variation of North American S. viridis correlates with both geography and climate and is representative of the total genetic diversity in this species. This pattern may reflect several introduction/dispersal events of S. viridis into North America. We also modelled demographic history and show signal of recent population decline in one subgroup. Finally, we show linkage disequilibrium decay is rapid (<45 kb) in our total sample and slow in genetic subgroups. These results together provide an in‐depth understanding of the pattern of genetic diversity of this new model species on a broad geographic scale. They also provide key guidelines for on‐going and future work including germplasm preservation, local adaptation, crossing designs and genomewide association studies.     

Links between prey assemblages and poison frog toxins: A landscape ecology approach to assess how biotic interactions affect species phenotypes

Ecological studies of species pairs showed that biotic interactions promote phenotypic change and eco‐evolutionary feedbacks. However, it is unclear how phenotypes respond to synergistic interactions with multiple taxa. We investigate whether interactions with multiple prey species explain spatially structured variation in the skin toxins of the neotropical poison frog Oophaga pumilio. Specifically, we assess how dissimilarity (i.e., beta diversity) of alkaloid‐bearing arthropod prey assemblages (68 ant species) and evolutionary divergence between frog populations (from a neutral genetic marker) contribute to frog poison dissimilarity (toxin profiles composed of 230 different lipophilic alkaloids sampled from 934 frogs at 46 sites). We find that models that incorporate spatial turnover in the composition of ant assemblages explain part of the frog alkaloid variation, and we infer unique alkaloid combinations across the range of O. pumilio. Moreover, we find that alkaloid variation increases weakly with the evolutionary divergence between frog populations. Our results pose two hypotheses: First, the distribution of only a few prey species may explain most of the geographic variation in poison frog alkaloids; second, different codistributed prey species may be redundant alkaloid sources. The analytical framework proposed here can be extended to other multitrophic systems, coevolutionary mosaics, microbial assemblages, and ecosystem services.     

Complex patterns of differentiation and gene flow underly the divergence of aposematic phenotypes in Oophaga poison frogs

Hybridization and introgression can have complex consequences for both species evolution and conservation. Here, we investigated the origin and characteristics of a putative hybrid zone between two South American poison dart frog species, Oophaga anchicayensis and the critically endangered Oophaga lehmanni, which are heavily sought after on the illegal pet market. Using a combination of phenotypic (49 traits) and genomic (ddRADseq) data, we found that the putative hybrids are morphologically distinct from their parental species and confirmed genomic signatures of admixture in these populations. Several lines of evidence (hybrid indices, interspecific hybrid heterozygosity, genomic clines, comparisons with simulated hybrids and demographic modelling) support the conclusion that these populations are not comprised of early‐generation hybrids and thus, they probably did not arise as a result of illegal translocations associated with wildlife trafficking. Instead, they probably represent an independent lineage which has persisted through isolation and has only relatively recently re‐established gene flow with both parental species. Furthermore, we detected signals of differential introgression from parental species into these hybrid populations which suggest relaxed stabilizing selection on these aposematic colour morphs, potentially via context‐dependent female choice. These populations thus provide a fascinating window into the role of hybridization, isolation and female choice in the diversification of South American poison dart frogs. In addition, our results underline the importance of landscape conservation measures to protect, not only known localities of nominal species, but also the phenotypic and genomic variation harbored by admixed lineages which represent crucial repositories for the impressive diversity in this system.     

Ecological and genetic divergence between two lineages of Middle American túngara frogs <Emphasis Type="Italic">Physalaemus</Emphasis> (= <Emphasis Type="Italic">Engystomops</Emphasis>) <Emphasis Type="Italic">pustulosus</Emphasis>

Background  

Uncovering how populations of a species differ genetically and ecologically is important for understanding evolutionary processes. Here we combine population genetic methods (microsatellites) with phylogenetic information (mtDNA) to define genetic population clusters of the wide-spread Neotropical túngara frog (Physalaemus pustulosus). We measure gene flow and migration within and between population clusters and compare genetic diversity between population clusters. By applying ecological niche modeling we determine whether the two most divergent genetic groups of the túngara frog (1) inhabit different habitats, and (2) are separated geographically by unsuitable habitat across a gap in the distribution.     

Radiation of the polymorphic Little Devil poison frog (Oophaga sylvatica) in Ecuador

Some South American poison frogs (Dendrobatidae) are chemically defended and use bright aposematic colors to warn potential predators of their unpalatability. Aposematic signals are often frequency‐dependent where individuals deviating from a local model are at a higher risk of predation. However, extreme diversity in the aposematic signal has been documented in poison frogs, especially in Oophaga. Here, we explore the phylogeographic pattern among color‐divergent populations of the Little Devil poison frog Oophaga sylvatica by analyzing population structure and genetic differentiation to evaluate which processes could account for color diversity within and among populations. With a combination of PCR amplicons (three mitochondrial and three nuclear markers) and genome‐wide markers from a double‐digested RAD (ddRAD) approach, we characterized the phylogenetic and genetic structure of 199 individuals from 13 populations (12 monomorphic and 1 polymorphic) across the O. sylvatica distribution. Individuals segregated into two main lineages by their northern or southern latitudinal distribution. A high level of genetic and phenotypic polymorphism within the northern lineage suggests ongoing gene flow. In contrast, low levels of genetic differentiation were detected among the southern lineage populations and support recent range expansions from populations in the northern lineage. We propose that a combination of climatic gradients and structured landscapes might be promoting gene flow and phylogenetic diversification. Alternatively, we cannot rule out that the observed phenotypic and genomic variations are the result of genetic drift on near or neutral alleles in a small number of genes.     

Genetic divergence and assortative mating between colour morphs of the sea urchin Paracentrotus gaimardi

Some species of sea urchins feature large variation in pigmentation. This variability may be the result of phenotypic plasticity or it may be associated with genetic divergence between morphs. Paracentrotus gaimardi exhibits five colour morphs (pink, brown, green, grey and black), which often occur side by side on the same rock. We studied genetic divergence between these morphs in three populations on the coast of Brazil. A fragment of the region encoding the mitochondrial ATPase 8 and 6 mitochondrial genes, a fragment of the intron of a nuclear histone and the entire nuclear gene coding for the sperm protein bindin were analysed. Mitochondrial DNA was differentiated between the pink and all other morphs, but the histone intron was similar in all colour morphs. In bindin, nine codons were found to be under positive selection and significant differences of allelic frequencies were observed in almost all pairwise comparisons between colour morphs. Although the molecular differentiation in bindin is not large enough to suggest reproductive isolation, some degree of assortative mating within morphs seems to be occurring in this species.     

Quaternary climate instability is correlated with patterns of population genetic variability in Bombus huntii

Climate oscillations have left a significant impact on the patterns of genetic diversity observed in numerous taxa. In this study, we examine the effect of Quaternary climate instability on population genetic variability of a bumble bee pollinator species, Bombus huntii in western North America. Pleistocene and contemporary B. huntii habitat suitability (HS) was estimated with an environmental niche model (ENM) by associating 1,035 locality records with 10 bioclimatic variables. To estimate genetic variability, we genotyped 380 individuals from 33 localities at 13 microsatellite loci. Bayesian inference was used to examine population structure with and without a priori specification of geographic locality. We compared isolation by distance (IBD) and isolation by resistance (IBR) models to examine population differentiation within and among the Bayesian inferred genetic clusters. Furthermore, we tested for the effect of environmental niche stability (ENS) on population genetic diversity with linear regression. As predicted, high‐latitude B. huntii habitats exhibit low ENS when compared to low‐latitude habitats. Two major genetic clusters of B. huntii inhabit western North America: (a) a north genetic cluster predominantly distributed north of 28°N and (b) a south genetic cluster distributed south of 28°N. In the south genetic cluser, both IBD and IBR models are significant. However, in the north genetic cluster, IBD is significant but not IBR. Furthermore, the IBR models suggest that low‐latitude montane populations are surrounded by habitat with low HS, possibly limiting dispersal, and ultimately gene flow between populations. Finally, we detected high genetic diversity across populations in regions that have been climatically unstable since the last glacial maximum (LGM), and low genetic diversity across populations in regions that have been climatically stable since the LGM. Understanding how species have responded to climate change has the potential to inform management and conservation decisions of both ecological and economic concerns.     

Global thermal niche models of two European grasses show high invasion risks in Antarctica

The two non‐native grasses that have established long‐term populations in Antarctica (Poa pratensis and Poa annua) were studied from a global multidimensional thermal niche perspective to address the biological invasion risk to Antarctica. These two species exhibit contrasting introduction histories and reproductive strategies and represent two referential case studies of biological invasion processes. We used a multistep process with a range of species distribution modelling techniques (ecological niche factor analysis, multidimensional envelopes, distance/entropy algorithms) together with a suite of thermoclimatic variables, to characterize the potential ranges of these species. Their native bioclimatic thermal envelopes in Eurasia, together with the different naturalized populations across continents, were compared next. The potential niche of P. pratensis was wider at the cold extremes; however, P. annua life history attributes enable it to be a more successful colonizer. We observe that particularly cold summers are a key aspect of the unique Antarctic environment. In consequence, ruderals such as P. annua can quickly expand under such harsh conditions, whereas the more stress‐tolerant P. pratensis endures and persist through steady growth. Compiled data on human pressure at the Antarctic Peninsula allowed us to provide site‐specific biosecurity risk indicators. We conclude that several areas across the region are vulnerable to invasions from these and other similar species. This can only be visualized in species distribution models (SDMs) when accounting for founder populations that reveal nonanalogous conditions. Results reinforce the need for strict management practices to minimize introductions. Furthermore, our novel set of temperature‐based bioclimatic GIS layers for ice‐free terrestrial Antarctica provide a mechanism for regional and global species distribution models to be built for other potentially invasive species.     

Genetic and Ecological Characterisation of Colour Dimorphism in a Coral Reef Fish

Synopsis Many recognised species of coral reef fishes exhibit two or more colour variants, but it is unknown whether these represent genetically identical phenotypes, genetic polymorphisms or closely related species. We tested between these alternatives for two colour morphs of the coral reef fish, Pseudochromis fuscus, from Lizard Island (Great Barrier Reef). A molecular analysis using mtDNA did not detect any genetic differentiation between co-occurring ‘yellow’ and ‘brown’ colour morphs. A previous study proposed that these two colour morphs are aggressive mimics of yellow and brown damselfishes. Here, a manipulative field experiment was used to evaluate whether the colour dimorphism in P. fuscus is a phenotypic response to the presence of two different model species. Colonies of either yellow or brown damselfish species were established on different patch reefs, and each of the two different P. fuscus morphs was then placed on the different reefs. Contrary to expectations, all yellow individuals that stayed on the reefs changed to brown, regardless of the model species. No brown individuals changed to the yellow colouration. However, P. fuscus were more likely to emigrate from, or suffer higher mortality on, patch reefs where they were not matched with similarly coloured models. Clearly, yellow and brown P. fuscus are members of a single species with sufficient phenotypic plasticity to switch from yellow to brown colouration.     

Phylogeography and ecological niche modeling unravel the evolutionary history of the African green toad,Bufotes boulengeri boulengeri (Amphibia: Bufonidae), through the Quaternary

Recent integration of ecological niche models in phylogeographic studies is improving our understanding of the processes structuring genetic variation across landscapes. Previous studies on the amphibian Bufotes boulengeri boulengeri uncovered a surprisingly weak intraspecific differentiation across the Maghreb region. We widely sampled this species from Morocco to Egypt and sequenced one nuclear and three mitochondrial (mtDNA) genes to determine the level of genetic variability across its geographic range. We evaluated these data with ecological niche modeling to reveal its evolutionary history in response to climate change during the Quaternary. Our results highlight some mtDNA phylogeographic structure within this species, with one haplogroup endemic to coastal Morocco, and one haplogroup widely distributed throughout North Africa. No or little genetic differentiation is observed between isolated populations from the Hoggar Mountains, the Sabha district and the islands of Kerkennah and Lampedusa, compared to others populations. This can be explained by the expansion of the distribution range of B. b. boulengeri during glacial periods. This might have facilitated the species’ dispersal and subsequent gene flow between most North African localities.     

Phylogeographic structure,demographic history and morph composition in a colour polymorphic lizard

In polymorphic species, population divergence in morph composition and frequency has the potential to promote speciation. We assessed the relationship between geographic variation in male throat colour polymorphism and phylogeographic structure in the tawny dragon lizard, Ctenophorus decresii. We identified four genetically distinct lineages, corresponding to two polymorphic lineages in the Northern Flinders Ranges and Southern Flinders Ranges/Olary Ranges regions respectively, and a monomorphic lineage in the Mt Lofty Ranges/Kangaroo Island region. The degree of divergence between these three lineages was consistent with isolation to multiple refugia during Pleistocene glacial cycles, whereas a fourth, deeply divergent (at the interspecific level) and monomorphic lineage was restricted to western New South Wales. The same four morphs occurred in both polymorphic lineages, although populations exhibited considerable variation in the frequency of morphs. By contrast, male throat coloration in the monomorphic lineages differed from each other and from the polymorphic lineages. Our results suggest that colour polymorphism has evolved once in the C. decresii species complex, with subsequent loss of polymorphism in the Mt Lofty Ranges/Kangaroo Island lineage. However, an equally parsimonious scenario, that polymorphism arose independently twice within C. decresii, could not be ruled out. We also detected evidence of a narrow contact zone with limited genotypic admixture between the polymorphic Olary Ranges and monomorphic Mt Lofty Ranges regions, yet no individuals of intermediate colour phenotype. Such genetic divergence and evidence for barriers to gene flow between lineages suggest incipient speciation between populations that differ in morph composition.     

The role of historical factors and natural selection in the evolution of breeding systems of Oxalis alpina in the Sonoran desert ‘Sky Islands’

Pleistocene climatic oscillations are known to influence the patterns of genetic diversity and the distribution of traits that are the target of selection. Here, we combine phylogeographical and ecological niche modelling (ENM) approaches to explore the influence of historical factors (Pleistocene climatic shifts) and natural selection on the evolution of distyly (two floral morphs) from tristyly (three floral morphs) of Oxalis alpina in the Sky Islands of the Sonoran Desert. Molecular data and ENM indicate that historical factors have had a strong influence on the genetic structure and the geographical distribution of reproductive systems of O. alpina. Moreover, genetic results suggest the possibility that distylous populations do not represent a monophyletic group. We propose that the combined effects of natural selection and genetic drift have influenced the tristyly–distyly transition.