Ian J. Wang

Isolation by environment

The interactions between organisms and their environments can shape distributions of spatial genetic variation, resulting in patterns of isolation by environment (IBE) in which genetic and environmental distances are positively correlated, independent of geographic distance. IBE represents one of the most important patterns that results from the ways in which landscape heterogeneity influences gene flow and population connectivity, but it has only recently been examined in studies of ecological and landscape genetics. Nevertheless, the study of IBE presents valuable opportunities to investigate how spatial heterogeneity in ecological processes, agents of selection and environmental variables contributes to genetic divergence in nature. New and increasingly sophisticated studies of IBE in natural systems are poised to make significant contributions to our understanding of the role of ecology in genetic divergence and of modes of differentiation both within and between species. Here, we describe the underlying ecological processes that can generate patterns of IBE, examine its implications for a wide variety of disciplines and outline several areas of future research that can answer pressing questions about the ecological basis of genetic diversity.

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.

Landscape genetics and least‐cost path analysis reveal unexpected dispersal routes in the California tiger salamander (Ambystoma californiense)

A major goal of landscape genetics is to understand how landscapes structure genetic variation in natural populations. However, landscape genetics still lacks a framework for quantifying the effects of landscape features, such as habitat type, on realized gene flow. Here, we present a methodology for identifying the costs of dispersal through different habitats for the California tiger salamander (Ambystoma californiense), an endangered species restricted to grassland/vernal pool habitat mosaics. We sampled larvae from all 16 breeding ponds in a geographically restricted area of vernal pool habitat at the Fort Ord Natural Reserve, Monterey County, California. We estimated between‐pond gene flow using 13 polymorphic microsatellite loci and constructed GIS data layers of habitat types in our study area. We then used least‐cost path analysis to determine the relative costs of movement through each habitat that best match rates of gene flow measured by our genetic data. We identified four measurable rates of gene flow between pairs of ponds, with between 10.5% and 19.9% of larvae having immigrant ancestry. Although A. californiense is typically associated with breeding ponds in grassland habitat, we found that dispersal through grassland is nearly twice as costly as dispersal through chaparral and that oak woodland is by far the most costly habitat to traverse. With the increasing availability of molecular resources and GIS data, we anticipate that these methods could be applied to a broad range of study systems, particularly those with cryptic life histories that make direct observation of movement challenging.

EXAMINING THE FULL EFFECTS OF LANDSCAPE HETEROGENEITY ON SPATIAL GENETIC VARIATION: A MULTIPLE MATRIX REGRESSION APPROACH FOR QUANTIFYING GEOGRAPHIC AND ECOLOGICAL ISOLATION

Understanding the effects of landscape heterogeneity on spatial genetic variation is a primary goal of landscape genetics. Ecological and geographic variables can contribute to genetic structure through geographic isolation, in which geographic barriers and distances restrict gene flow, and ecological isolation, in which gene flow among populations inhabiting different environments is limited by selection against dispersers moving between them. Although methods have been developed to study geographic isolation in detail, ecological isolation has received much less attention, partly because disentangling the effects of these mechanisms is inherently difficult. Here, I describe a novel approach for quantifying the effects of geographic and ecological isolation using multiple matrix regression with randomization. I explored the parameter space over which this method is effective using a series of individual‐based simulations and found that it accurately describes the effects of geographic and ecological isolation over a wide range of conditions. I also applied this method to a set of real‐world datasets to show that ecological isolation is an often overlooked but important contributor to patterns of spatial genetic variation and to demonstrate how this analysis can provide new insights into how landscapes contribute to the evolution of genetic variation in nature.

Quantifying the roles of ecology and geography in spatial genetic divergence

Investigating the properties of ecological landscapes that influence gene flow among populations can provide key insights into the earliest stages of biological divergence. Both ecological and geographical factors can reduce gene flow, which can lead to population divergence, but we know little of the relative strengths of these phenomena in nature. Here, we use a novel application of structural equation modelling to quantify the contributions of ecological and geographical isolation to spatial genetic divergence in 17 species of Anolis lizards. Our comparative analysis shows that although both processes contributed significantly, geographical isolation explained substantially more genetic divergence than ecological isolation (36.3 vs. 17.9% of variance respectively), suggesting that despite the proposed ubiquity of ecological divergence, non-ecological factors play the dominant role in the evolution of spatial genetic divergence.

Recognizing the temporal distinctions between landscape genetics and phylogeography

The steadily advancing fields of landscape genetics and phylogeography share many goals. However, there are some very distinct differences between these two disciplines, including the kinds of data and analyses commonly used, the timescale over which these data are informative, and the hypotheses the data are used to examine. Recently, a number of studies appear to have confused or synonymized phylogeography and landscape genetics. The difference is not merely semantic; understanding the distinctions between these fields is important for ensuring that researchers are aware of the temporal scale over which their data are informative.

Genome-enabled development of DNA markers for ecology, evolution and conservation.

Molecular markers have become a fundamental piece of modern biology’s toolkit. In the last decade, new genomic resources from model organisms and advances in DNA sequencing technology have altered the way that these tools are developed, alleviating the marker limitation that researchers previously faced and opening new areas of research for studies of non‐model organisms. This availability of markers is directly responsible for advances in several areas of research, including fine‐scaled estimation of population structure and demography, the inference of species phylogenies, and the examination of detailed selective pressures in non‐model organisms. This review summarizes methods for the development of large numbers of DNA markers in non‐model organisms, the challenges encountered when utilizing different methods, and new research applications resulting from these advances.

Rapid Color Evolution in an Aposematic Species: A Phylogenetic Analysis of Color Variation in the Strikingly Polymorphic Strawberry Poison-dart Frog

Abstract Aposematism is one of the great mysteries of evolutionary biology. The evolution of aposematic coloration is poorly understood, but even less understood is the evolution of polymorphism in aposematic signals. Here, we use a phylogeographic approach to investigate the evolution of color polymorphism in Dendrobates pumilio, a well-known poison-dart frog (family Dendrobatidae), which displays perhaps the most striking color variation of any aposematic species. With over a dozen color morphs, ranging from bright red to dull green, D. pumilio provides an ideal opportunity to examine the evolution of color polymorphism and evolutionary shifts to cryptic coloration in an otherwise aposematic species. We constructed a phylogenetic tree for all D. pumilio color morphs from 3051bp of mtDNA sequence data, reconstructed ancestral states using parsimony and Bayesian methods, and tested the recovered tree against constraint trees using parametric bootstrapping to determine the number of changes to each color type. We find strong evidence for nearly maximal numbers of changes in all color traits, including five independent shifts to dull dorsal coloration. Our results indicate that shifts in coloration in aposematic species may occur more regularly than predicted and that convergence in coloration may indicate that similar forces are repeatedly driving these shifts.

Fine‐scale population structure in a desert amphibian: landscape genetics of the black toad (Bufo exsul)

Environmental variables can strongly influence a variety of intra‐ and inter‐population processes, including demography, population structure and gene flow. When environmental conditions are particularly harsh for a certain species, investigating these effects is important to understanding how populations persist under difficult conditions. Furthermore, species inhabiting challenging environments present excellent opportunities to examine the effects of complex landscapes on population processes because these effects will often be more pronounced. In this study, I use 16 microsatellite loci to examine population structure, gene flow and demographic history in the black toad, Bufo exsul, which has one of the most restricted natural ranges of any amphibian. Bufo exsul inhabits four springs in the Deep Springs Valley high desert basin and has never been observed more than several meters from any source of water. My results reveal limited gene flow and moderately high levels of population structure (FST = 0.051–0.063) between all but the two closest springs. I found that the geographic distance across the arid scrub habitat between springs is significantly correlated with genetic structure when distance accounts for topography and barriers to dispersal. I also found very low effective population sizes (Ne = 7–30) and substantial evidence for historical population bottlenecks in all four populations. Together, these results suggest that the desert landscape and B. exsul’s high habitat specificity contribute significantly to population structure and demography in this species and emphasize the importance of considering behavioural and landscape data in conservation genetic studies of natural systems.

Phylogeography of the Pygmy Rain Frog (Pristimantis ridens) across the lowland wet forests of isthmian Central America

We used a phylogeographic approach to elucidate the evolutionary history of a lineage of frogs, known as Pristimantis (formerly Eleutherodactylus) ridens (Anura: Brachycephalidae), restricted to the wet forests occurring along the Caribbean versant of isthmian Central America as well as the disjunct wet forest on the Pacific slope of Costa Rica. We placed our phylogeographic study of P. ridens within a larger molecular phylogenetic analysis of Central American Pristimantis. All phylogenetic inferences were based on a 1455 base pair fragment of mitochondrial DNA, containing the complete ND2 gene and five flanking tRNA genes. Our reconstruction of the intraspecific phylogeny of P. ridens yielded a basal trichotomy dating to an estimated 12+ million years ago (Ma), consisting of central Panama, western Panama, and Costa Rica plus Honduras. Thus, the presence of P. ridens appears to predate the completion of the Isthmus 3.1Ma. Using a parametric bootstrap (SOWH) test, we evaluated four a priori zoogeographic hypotheses for the origin and spread of P. ridens. This analysis suggested that the P. ridens populations on the Caribbean versant of Costa Rica were established by Pacific versant ancestors only recently, in contrast to the very old lineages found in Panama. Our results support a model of Miocene colonization, long-term geographic stasis, followed by rapid dispersal across the Caribbean lowlands during the Pliocene or Pleistocene.