Adding more ecology into species delimitation: ecological niche models and phylogeography help define cryptic species in the black salamander (Aneides flavipunctatus)

Being able to efficiently and accurately delimit species is one of the most basic and important aspects of systematics because species are the fundamental unit of analysis in biogeography, ecology, and conservation. We present a rationale and approach for combining ecological niche modeling, spatially explicit analyses of environmental data, and phylogenetics in species delimitation, and we use our methodology in an empirical example focusing on Aneides flavipunctatus, the black salamander (Caudata: Plethodontidae), in California. We assess the relationships between genetic, environmental, and geographic distance among populations. We use 11 climatic variables and point locality data from public databases to create ecological niche models. The suitability of potential contact zones between parapatric lineages is also assessed using the data from ecological niche modeling. Phylogenetic analyses of portions of the mitochondrial genome reveal morphologically cryptic mitochondrial lineages in this species. In addition, we find that patterns of genetic divergence are strongly associated with divergence in the ecological niche. Our work demonstrates the ease and utility of using spatial analyses of environmental data and phylogenetics in species delimitation, especially for groups displaying fine-scaled endemism and cryptic species.     

Reconciling phylogeography and ecological niche models for New Zealand beetles: Looking beyond glacial refugia

Mitochondrial DNA (cox1) sequence data and recently developed coalescent phylogeography models were used to construct geo-spatial histories for the New Zealand fungus beetles Epistranus lawsoni and Pristoderus bakewelli (Zopheridae). These methods utilize continuous-time Markov chains and Bayesian stochastic search variable selection incorporated in BEAST to identify historical dispersal patterns via ancestral state reconstruction. Ecological niche models (ENMs) were incorporated to reconstruct the potential geographic distribution of each species during the Last Glacial Maximum (LGM). Coalescent analyses suggest a North Island origin for E. lawsoni, with gene flow predominately north-south between adjacent regions. ENMs for E. lawsoni indicated glacial refugia in coastal regions of both main islands, consistent with phylogenetic patterns but at odds with the coalescent dates, which implicate much older topographic events. Dispersal matrices revealed patterns of gene flow consistent with projected refugia, suggesting long-term South Island survival with population vicariance around the Southern Alps. Phylogeographic relationships are more ambiguous for P. bakewelli, although long-term survival on both main islands is evident. Divergence dates for both species are consistent with the topographic evolution of New Zealand over the last 10Ma, whereas the signature of the LGM is less apparent in the time-scaled phylogeny.     

Integrating coalescent and ecological niche modeling in comparative phylogeography

Understanding the factors that contribute to the formation of population genetic structure is a central goal of phylogeographic research, but achieving this goal can be complicated by the stochastic variance inherent to genetic processes. Statistical approaches to testing phylogeographic hypotheses accommodate this stochasticity by evaluating competing models of putative historical population structure, often by simulating null distributions of the expected variance. The effectiveness of these tests depends on the biological realism of the models. Information from the fossil record can aid in reconstructing the historical distributions of some taxa. However, for the majority of taxa, which lack sufficient fossils, paleodistributional modeling can provide valuable spatial-geographic data concerning ancestral distributions. Paleodistributional models are generated by projecting ecological niche models, which predict the current distribution of each species, onto a model of past climatic conditions. Here, we generate paleodistributional models describing the suitable habitat during the last glacial maximum for lineages from the mesic forests of the Pacific Northwest of North America, and use these models to generate alternative phylogeographic hypotheses. Coalescent simulations are then used to test these hypotheses to improve our understanding of the historical events that promoted the formation of population genetic structure in this ecosystem. Results from Pacific Northwest mesic forest organisms demonstrate the utility of these combined approaches. Paleodistribution models and population genetic structure are congruent across three amphibian lineages, suggesting that they have responded in a concerted manner to environmental change. Two other species, a willow and a water vole, despite being currently codistributed and having similar population genetic structure, were predicted by the paleodistributional model to have had markedly different distributions during the last glacial maximum. This suggests that congruent phylogeographic patterns can arise from incongruent ancestral distributions. Paleodistributional models introduce a much-needed spatial-geographic perspective to statistical phylogeography. In conjunction with coalescent models of population genetic structure, they have the potential to improve our understanding of the factors that promote population divergence and ultimately produce regional patterns of biodiversity.     

Ecological niche variation in the Wilson's warbler Cardellina pusilla complex

Wilson's warbler comprises three subspecies separated into two geographic groups: C. p. pusilla that breeds in eastern North America; and C. p. pileolata and C. p. chryseola that breed in western North America. Given the differences between the groups in genetics, morphology, habitat use, and population decline, we tested for ecological niche similarity in both their breeding and wintering distribution using niche modeling based on temperature and precipitation data. We first conducted an inter‐prediction approach considering the percent of summer and winter localities of one group that are predicted by the potential distribution of the alternate group. We also applied a null model approach that compares self‐predictions and pseudoreplicates of each group to indicate similarity, divergence, or indeterminate niche overlap. Finally, we compared ecological distances between and within groups using the Gower similarity equation. We found that the western group had an ecological niche of broader climatic conditions, while the eastern group had a narrower ecological niche. The inter‐prediction approach showed that, for both summering and wintering ranges, ecological niche models of the western group predicted ～50% of the observed distribution of the eastern group, whereas eastern group models predicted < 18% of the western group distribution. The null model approach found that similarity in ecological niches was indeterminate, possibly due to the large area occupied by the two groups; but it suggests a more restricted set of climatic conditions of the eastern group distribution. However, the Gower coefficients demonstrated that the ecological distance between the two geographic groups was larger than the ecological distance within groups, indicating distinct ecological niches. Overall, our results support the hypothesis that the eastern and western groups of Wilson's warbler are two cryptic species; this should be taken into consideration for future analyses, particularly with respect to vulnerability categorization and conservation efforts.     

Speciation in mountain refugia: phylogeography and demographic history of the pine siskin and black‐capped siskin complex

Following Pleistocene glacial maxima, species that adapted to temperate climates in low‐latitude refugia had to modify their ranges as climate changed, expanding either latitudinally towards the poles, or altitudinally to higher elevations in mountainous regions. Within just a few thousand years, populations taking alternative routes during interglacials became isolated from each other and subjected to different selection pressures, often leading to lineage divergence and speciation. The pine siskin Spinus pinus is a common and widespread songbird showing relative phenotypic uniformity across the North American continent. One exception is the subspecies found in the highlands of northern Central America (S. p. perplexus), which shows marked differentiation in plumage color and shares some traits with the endemic and partly sympatric black‐capped siskin S. atriceps, suggesting potential introgression or even a hybrid origin of perplexus. Relationships and species limits among pinus, perplexus and atriceps have been controversial for decades. We provide new molecular evidence to help resolve the evolutionary history of the group. Phylogenetic analysis of mitochondrial DNA and nuclear intron sequences revealed three distinct lineages within the complex, corresponding to: 1) S. pinus individuals from Canada through central Mexico (S. p. pinus and S. p. macropterus), 2) individuals from the highlands of Guatemala and Chiapas (S. p. perplexus), and 3) S. atriceps. Pine siskins across North America show evidence of a recent postglacial population expansion and extremely low levels of diversity and structure. In contrast, S. p. perplexus shows evidence of demographic stasis, reflecting long‐term isolation and restricted dispersal. Marked and diagnostic genetic differences among the three lineages in mtDNA and at least one intron, suggest that a hybrid origin of S. p. perplexus is unlikely, yet some degree of introgression between S. p. perplexus and S. atriceps cannot be ruled out in localities where they occur in sympatry.     

Investigating niche and lineage diversification in widely distributed taxa: phylogeography and ecological niche modeling of the Peromyscus maniculatus species group

The relationship between lineage formation and variation in the ecological niche is a fundamental evolutionary question. Two prevailing hypotheses reflect this relationship: niche conservatism and niche divergence. Niche conservatism predicts a pattern where sister taxa will occupy similar niche spaces; whereas niche divergence predicts that sister taxa will occupy different niche spaces. Widely distributed species often show distinct phylogeographic structure, but little research has been conducted on how the environment may be related to these phylogenetic patterns. We investigated the relationship between lineage divergence and environmental space for the closely related species Peromyscus maniculatus and P. polionotus utilizing phylogenetic techniques and ecological niche modeling (ENM). We estimated the phylogenetic relationship among individuals based on complete cytochrome b sequences that represent individuals from a majority of the species ranges. Niche spaces that lineages occupy were estimated by using 12 environmental layers. Differences in niche space were tested using multivariate statistics based on location data, and ENMs were employed using maximum entropy algorithms. Two similarity indices estimated significant divergence in environmental space based on the ENM. Six geographically structured lineages were identified within P. maniculatus. Nested within P. maniculatus we found that P. polionotus recently diverged from a clade occupying central and western United States. We estimated that the majority of the genetic lineages occupy distinct environmental niches, which supports a pattern of niche divergence. Two sister taxa showed niche divergence and represent different ecomorphs, suggesting morphological, genetic and ecological divergence between the two lineages. Two other sister taxa were observed in the same environmental space based on multivariate statistics, suggesting niche conservatism. Overall our results indicate that a widely distributed species may exhibit both niche conservatism and niche divergence, and that most lineages seem to occupy distinct environmental niches.     

Whole-genome sequencing reveals a complex African population demographic history and signatures of local adaptation

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Quaternary range and demographic expansion of Liolaemus darwinii (Squamata: Liolaemidae) in the Monte Desert of Central Argentina using Bayesian phylogeography and ecological niche modelling

Until recently, most phylogeographic approaches have been unable to distinguish between demographic and range expansion processes, making it difficult to test for the possibility of range expansion without population growth and vice versa. In this study, we applied a Bayesian phylogeographic approach to reconstruct both demographic and range expansion in the lizard Liolaemus darwinii of the Monte Desert in Central Argentina, during the Late Quaternary. Based on analysis of 14 anonymous nuclear loci and the cytochrome b mitochondrial DNA gene, we detected signals of demographic expansion starting at ~55 ka based on Bayesian Skyline and Skyride Plots. In contrast, Bayesian relaxed models of spatial diffusion suggested that range expansion occurred only between ~95 and 55 ka, and more recently, diffusion rates were very low during demographic expansion. The possibility of population growth without substantial range expansion could account for the shared patterns of demographic expansion during the Last Glacial Maxima (OIS 2 and 4) in fish, small mammals and other lizards of the Monte Desert. We found substantial variation in diffusion rates over time, and very high rates during the range expansion phase, consistent with a rapidly advancing expansion front towards the southeast shown by palaeo‐distribution models. Furthermore, the estimated diffusion rates are congruent with observed dispersal rates of lizards in field conditions and therefore provide additional confidence to the temporal scale of inferred phylogeographic patterns. Our study highlights how the integration of phylogeography with palaeo‐distribution models can shed light on both demographic and range expansion processes and their potential causes.     

Southward Pleistocene migration of Douglas-fir into Mexico: phylogeography, ecological niche modeling, and conservation of 'rear edge' populations

? Poleward Pleistocene plant migration has been an important process structuring modern temperate and boreal plant communities, but the contribution of equatorward migration remains poorly understood. Paleobotanical evidence suggests Miocene or Pleistocene origin for temperate 'sky island' plant taxa in Mexico. These 'rear edge' populations situated in a biodiversity hotspot may be an important reserve of genetic diversity in changing climates. ? We used mtDNA sequences, cpDNA sequences and chloroplast microsatellites to test hypotheses of Miocene vs Pleistocene colonization of temperate Douglas-fir in Mexico, explore geographic patterns of molecular variation in relation to Pleistocene climate history using ecological niche models, and assess the taxonomic and conservation implications. ? We found strong evidence for Pleistocene divergence of Douglas-fir in Mexico (958 thousand yr before present (ka) with the 90% highest posterior density interval ranging from 1.6 million yr before present (Ma) to 491 ka), consistent with the southward Pleistocene migration hypothesis. Genetic diversity was high and strongly partitioned among populations. Spatial patterns of molecular variation and ecological niche models suggest a complex late Pleistocene history involving periods of isolation and expansion along mountain corridors. ? These results highlight the importance of southward Pleistocene migration in establishing modern high-diversity plant communities and provide critical insights into proposals to conserve the unique biodiversity of Mexican Douglas-fir and associated taxa.     

Comparative phylogeography and demographic history of two marsupials of the Atlantic Forest in eastern Brazil

The Atlantic Forest biodiversity hotspot in eastern South America has been the focus of several phylogeographic studies concerning relationships between populations and areas and how taxa respond to environmental changes. We infer and compare the demographic and biogeographic histories of two didelphid marsupial species, Gracilinanus microtarsus and Marmosops incanus, from the Atlantic Forest of eastern Brazil to determine how these species responded to environmental changes over time, using mitochondrial and nuclear DNA sequences. We found great intraspecific genetic divergence in both species and a strong geographic structure related to similar and spatially cohesive groups within each species. These groups are consistent with the same topographical barriers, such as mountains and river valleys. Intraspecific clades are very old, dating back to a period of tectonic activities in the Neogene (5.39–8.57 Mya). Changes in the environment over the last 7 million years lead to fairly concordant demographic changes in both marsupial species, including population expansion during the last glacial maximum (ca. 21,000 years ago) or last interglacial (ca. 120,000 years ago) or both. These results do not fit the Pleistocene refuge hypothesis as an explanation of the historical biogeography and diversification of both species in the Atlantic Forest, but are compatible with the Atlantis Forest hypothesis.     

Correlation between genetic diversity and environmental suitability: taking uncertainty from ecological niche models into account

The hindcast of shifts in the geographical ranges of species as estimated by ecological niche modelling (ENM) has been coupled with phylogeographical patterns, allowing the inference of past processes that drove population differentiation and genetic variability. However, more recently, some studies have suggested that maps of environmental suitability estimated by ENM may be correlated to species' abundance, raising the possibility of using environmental suitability to infer processes related to population demographic dynamics and genetic variability. In both cases, one of the main problems is that there is a wide variation in ENM development methods and climatic models. In this study, we analyse the relationship between heterozygosity (He) and environmental suitability from multiple ENMs for 25 population estimates for Dipteryx alata, a widely distributed, endemic tree species of the Cerrado region of central Brazil. We propose a new approach for generating a statistical distribution of correlations under randomly generated ENM. The confidence intervals from these distributions indicate how model selection with different properties affects the ability to detect a correlation of interest (e.g. the correlation between He and suitability). Additionally, our approach allows us to explore which particular ensemble of ENMs produces the better result for finding an association between environmental suitability and He. Caution is necessary when choosing a method or a climatic data set for modelling geographical distributions, but the new approach proposed here provides a conservative way to evaluate the ability of ensembles to detect patterns of interest.     

Pliocene–Pleistocene ecological niche evolution shapes the phylogeography of a Mediterranean plant group

Estimating species ability to adapt to environmental changes is crucial to understand their past and future response to climate change. The Mediterranean Basin has experienced remarkable climatic changes since the Miocene, which have greatly influenced the evolution of the Mediterranean flora. Here, we examine the evolutionary history and biogeographic patterns of two sedge sister species (Carex, Cyperaceae) restricted to the western Mediterranean Basin, but with Pliocene fossil record in central Europe. In particular, we estimated the evolution of climatic niches through time and its influence in lineage differentiation. We carried out a dated phylogenetic–phylogeographic study based on seven DNA regions (nDNA and ptDNA) and fingerprinting data (AFLPs), and modelled ecological niches and species distributions for the Pliocene, Pleistocene and present. Phylogenetic and divergence time analyses revealed that both species form a monophyletic lineage originated in the late Pliocene–early Pleistocene. We detected clear genetic differentiation between both species with distinct genetic clusters in disjunct areas, indicating the predominant role of geographic barriers limiting gene flow. We found a remarkable shift in the climatic requirements between Pliocene and extant populations, although the niche seems to have been relatively conserved since the Pleistocene split of both species. This study highlights how an integrative approach combining different data sources and analyses, including fossils, allows solid and robust inferences about the evolutionary history of a plant group since the Pliocene.     

Comparative phylogeography and demographic history of the wood lemming (Myopus schisticolor): implications for late Quaternary history of the taiga species in Eurasia

The association between demographic history, genealogy and geographical distribution of mitochondrial DNA cytochrome b haplotypes was studied in the wood lemming (Myopus schisticolor), a species that is closely associated with the boreal forest of the Eurasian taiga zone from Scandinavia to the Pacific coast. Except for a major phylogeographic discontinuity (0.9% nucleotide divergence) in southeastern Siberia, only shallow regional genetic structure was detected across northern Eurasia. Genetic signs of demographic expansions imply that successive range contractions and expansions on different spatial scales represented the primary historical events that shaped geographical patterns of genetic variation. Comparison of phylogeographic structure across a taxonomically diverse array of other species that are ecologically associated with the taiga forest revealed similar patterns and identified two general aspects. First, the major south-north phylogeographic discontinuity observed in five out of six species studied in southeastern Siberia and the Far East implies vicariant separation in two different refugial areas. The limited distribution range of the southeastern lineages provides no evidence of the importance of the putative southeastern refugial area for postglacial colonization of northern Eurasia by boreal forest species. Second, the lack of phylogeographic structure associated with significant reciprocal monophyly and genetic signatures of demographic expansion in all nine boreal forest animal species studied to date across most of northern Eurasia imply contraction of each species to a single refugial area during the late Pleistocene followed by range expansion on a continental scale. Similar phylogeographic patterns observed in this taxonomically diverse set of organisms with different life histories and dispersal potentials reflect the historical dynamics of their shared environment, the taiga forest in northern Eurasia.     

Evaluating alternative data sets for ecological niche models of birds in the Andes

Ecological niche modeling (ENM) is an effective tool for providing innovative insights to questions in evolution, ecology and conservation. As environmental datasets accumulate, modelers need to evaluate the relative merit of different types of data for ENM. We used three alternative environmental data sets: climatic data, remote-sensing data (Normalized Difference Vegetation Index), and elevation data, to model the distribution of six bird species of the genus Grallaria in the Ecuadorian Andes. We assessed the performance of models created with each environmental data set and all possible combinations by comparing the geographic predictions of our models with detailed maps developed by expert ornithologists. Results varied depending on the specific measure of performance. Models including climate variables performed relatively well across most measures, whereas models using only NDVI performed poorly. Elevation based models were relatively good at predicting most sites of expected occurrence but showed a high over-prediction error. Combinations of data sets usually increased the performance of the models, but not significantly. Our results highlight the importance of including climatic variables in ENM and the simultaneous use of various data sets when possible. This strategy attenuates the effects of specific variables that decrease model performance. Remote-sensing data, such as NDVI, should be used with caution in topographically complex regions with heavy cloud-cover. Nonetheless, remote-sensing data have the potential to improve ENM. Finally, we suggest a priori designation of modeling purposes to define specific performance measures accordingly.     

Comparative phylogeography of five widespread tree species: Insights into the history of western Amazonia

Various historical processes have been put forth as drivers of patterns in the spatial distribution of Amazonian trees and their population genetic variation. We tested whether five widespread tree species show congruent phylogeographic breaks and similar patterns of demographic expansion, which could be related to proposed Pleistocene refugia or the presence of geological arches in western Amazonia. We sampled Otoba parvifolia/glycycarpa (Myristicaceae), Clarisia biflora, Poulsenia armata, Ficus insipida (all Moraceae), and Jacaratia digitata (Caricaceae) across the western Amazon Basin. Plastid DNA (trnH–psbA; 674 individuals from 34 populations) and nuclear ribosomal internal transcribed spacers (ITS; 214 individuals from 30 populations) were sequenced to assess genetic diversity, genetic differentiation, population genetic structure, and demographic patterns. Overall genetic diversity for both markers varied among species, with higher values in populations of shade‐tolerant species than in pioneer species. Spatial analysis of molecular variance (SAMOVA) identified three genetically differentiated groups for the plastid marker for each species, but the areas of genetic differentiation were not concordant among species. Fewer SAMOVA groups were found for ITS, with no detectable genetic differentiation among populations in pioneers. The lack of spatially congruent phylogeographic breaks across species suggests no common biogeographic history of these Amazonian tree species. The idiosyncratic phylogeographic patterns of species could be due instead to species‐specific responses to geological and climatic changes. Population genetic patterns were similar among species with similar biological features, indicating that the ecological characteristics of species impact large‐scale phylogeography.     

Integrating microbial ecology into ecosystem models: challenges and priorities

Microbial communities can potentially mediate feedbacks between global change and ecosystem function, owing to their sensitivity to environmental change and their control over critical biogeochemical processes. Numerous ecosystem models have been developed to predict global change effects, but most do not consider microbial mechanisms in detail. In this idea paper, we examine the extent to which incorporation of microbial ecology into ecosystem models improves predictions of carbon (C) dynamics under warming, changes in precipitation regime, and anthropogenic nitrogen (N) enrichment. We focus on three cases in which this approach might be especially valuable: temporal dynamics in microbial responses to environmental change, variation in ecological function within microbial communities, and N effects on microbial activity. Four microbially-based models have addressed these scenarios. In each case, predictions of the microbial-based models differ—sometimes substantially—from comparable conventional models. However, validation and parameterization of model performance is challenging. We recommend that the development of microbial-based models must occur in conjunction with the development of theoretical frameworks that predict the temporal responses of microbial communities, the phylogenetic distribution of microbial functions, and the response of microbes to N enrichment.