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.     

An information-theoretical approach to phylogeography

Data analysis in phylogeographic investigations is typically conducted in either a qualitative manner, or alternatively via the testing of null hypotheses. The former, where inferences about population processes are derived from geographical patterns of genetic variation, may be subject to confirmation bias and prone to overinterpretation. Testing the predictions of null hypotheses is arguably less prone to bias than qualitative approaches, but only if the tested hypotheses are biologically meaningful. As it is difficult to know a priori if this is the case, there is the general need for additional methodological approaches in phylogeographic research. Here, we explore an alternative method for analysing phylogeographic data that utilizes information theory to quantify the probability of multiple hypotheses given the data. We accomplish this by augmenting the model‐selection procedure implemented in ima with calculations of Akaike Information Criterion scores and model probabilities. We generate a ranking of 17 models each representing a set of historical evolutionary processes that may have contributed to the evolution of Plethodon idahoensis, and then quantify the relative strength of support for each hypothesis given the data using metrics borrowed from information theory. Our results suggest that two models have high probability given the data. Each of these models includes population divergence and estimates of ancestral θ that differ from estimates of descendent θ, inferences consistent with prior work in this system. However, the models disagree in that one includes migration as a parameter and one does not, suggesting that there are two regions of parameter space that produce model likelihoods that are similar in magnitude given our data. Results of a simulation study suggest that when data are simulated with migration, most of the optimal models include migration as a parameter, and further that when all of the shared polymorphism results from incomplete lineage sorting, most of the optimal models do not. The results could also indicate a lack of precision, which may be a product of the amount of data that we have collected. In any case, the information‐theoretic metrics that we have applied to the analysis of our data are statistically rigorous, as are hypothesis‐testing approaches, but move beyond the ‘reject/fail to reject’ dichotomy of conventional hypothesis testing in a manner that provides considerably more flexibility to researchers.     

Fine-scale comparative phylogeography of a sympatric sister species triplet of subterranean diving beetles from a single calcrete aquifer in Western Australia

Calcrete aquifers in the arid Yilgarn region of central Western Australia are a biodiversity hotspot for stygofauna. A distinct pattern of interspecific size class variation among subterranean dytiscid beetle species has been observed in 29 of these aquifers where either two or three small, medium and/or large sympatric species are found that are in some cases sister species. We used a 3.5 km² grid of bores to sample dytiscids on a fine-scale and employed a comparative phylogeographical and population genetic approach to investigate the origins of a sympatric sister species triplet of diving beetles from a single aquifer. Mitochondrial DNA sequence data from the Cytochrome oxidase c subunit I gene revealed that all three species have high levels of haplotype diversity with ancient (∼1 million years ago) intra-specific coalescence of haplotypes, but low levels of nucleotide diversity. Population analyses provide evidence for multiple expansion events within each species. There was spatial heterogeneity in the distribution of genetic variation and abundance both within and among the three taxa. Population analyses revealed significant fine-scale differentiation with isolation by distance for Paroster macrosturtensis and P. mesosturtensis , but not the smallest species P. microsturtensis . Haplotype network analyses provided limited or no evidence for past population fragmentation within the large and small species, but substantial historical divergence was observed in P. mesosturtensis that was not spatially structured. A patchy population structure with contemporaneous and historical isolation by distance in the three species is likely to have been a significant isolating and diversifying force, preventing us from ruling out a potential role for allopatric divergence during speciation of this beetle sister triplet.     

Comparative phylogeography as an integrative approach to historical biogeography

Phylogeography has become a powerful approach for elucidating contemporary geographical patterns of evolutionary subdivision within species and species complexes. A recent extension of this approach is the comparison of phylogeographic patterns of multiple co-distributed taxonomic groups, or 'comparative phylogeography.' Recent comparative phylogeographic studies have revealed pervasive and previously unrecognized biogeographic patterns which suggest that vicariance has played a more important role in the historical development of modern biotic assemblages than current taxonomy would indicate. Despite the utility of comparative phylogeography for uncovering such 'cryptic vicariance', this approach has yet to be embraced by some researchers as a valuable complement to other approaches to historical biogeography. We address here some of the common misconceptions surrounding comparative phylogeography, provide an example of this approach based on the boreal mammal fauna of North America, and argue that together with other approaches, comparative phylogeography can contribute importantly to our understanding of the relationship between earth history and biotic diversification.     

A comparative psychophysical approach to visual perception in primates

Studies on the visual processing of primates, which have well developed visual systems, provide essential information about the perceptual bases of their higher-order cognitive abilities. Although the mechanisms underlying visual processing are largely shared between human and nonhuman primates, differences have also been reported. In this article, we review psychophysical investigations comparing the basic visual processing that operates in human and nonhuman species, and discuss the future contributions potentially deriving from such comparative psychophysical approaches to primate minds.     

Species diversification and phylogeographical patterns of birds in response to the uplift of the Qinghai-Tibet Plateau and Quaternary glaciations

The Qinghai-Tibet Plateau （QTP） is well known for being of great importance in the evolution of montane species due to its unique geological history and landform configuration, climate complexity, and diversified habitats. The effect of environmental changes since the Quaternary on species diversification, population genetic structure, and demography under environmental change can be studied using phylogenetic and phylogeographieal approaches. Birds are the most well-studied group of all terrestrial vertebrates with regard to their response to climatic changes over time. Herein, we briefly review the species diversification of birds in response to the uplift of the QTP, focusing on summarizing the different phylogeographical patterns of birds on the Plateau, its southeastern margin, and the Eastern Himalayas and the reasons underlying these patterns. Speciation was found to be closely related to the uplift of the QTP, with different patterns of intraspecific processes： （1） no divergence within a single refuge was identified in a restricted semi-continuous area of the eastern margin of the Plateau; （2） two divergent lineages with separated refugia were located at the south-eastern and north-eastern margins of the plateau; and （3） multiple divergent lineages within subregions were found in the Eastern Himalayas. Glacial movements and induced climate change are considered to be key factors in shaping these different patterns. The species distributed mainly in the heavily ice-covered platform regions of the Plateau experienced population expansion following the retreat of the extensive glaciations, whereas the species distributed on the ice-free edges of the plateau maintained their population size at a stable level. Demographic stresses on the edge species might have been mitigated by the milder climate in comparison to their platform-distributed counterparts. Various behavioral and ecological characteristics, including dispersal capacity, habitat preference, and elevation specificity, along with evolutionary history might have helped to shape these different phylogeographical patterns [Current Zoology 60 （2）： 149-161, 2014].     

Comparative phylogeography of West African amphibians and reptiles

Comparative phylogeographic studies often support shared divergence times for co-distributed species with similar life histories and habitat specializations. During the late Holocene, West Africa experienced aridification and the turnover of rain forest habitats into savannas. These fragmented rain forests harbor impressive numbers of endemic and threatened species. In this setting, populations of co-distributed rain forest species are expected to have diverged simultaneously, whereas divergence events for species adapted to savanna and forest-edge habitats should be absent or idiosyncratic. We conducted a Bayesian analysis of shared evolutionary events to test models of population divergence for 20 species of anurans (frogs) and squamates (lizards and snakes) that are distributed across the Dahomey Gap, a climate change-induced savanna barrier responsible for fragmenting previously contiguous rain forests of Ghana into two regions: the Togo-Volta Hills and the Southwestern Forests. A model of asynchronous diversification is supported for anurans and squamates, suggesting that drivers of diversification are not specifically related to ecological and life history associations with habitat types. Instead, the wide variability of genetic divergence histories exhibited by these species suggests that biodiversity in this region has been shaped by diversification events that extend beyond the Holocene. Comparisons of the genealogical divergence index, a measure of the genetic divergence between populations due to the combined effects of genetic isolation and gene flow, illustrate that these populations represent a broad sampling of the speciation continuum.     

A molecular phylogeography approach to biological invasions of the New World by parthenogenetic Thiarid snails

The parthenogenetic snail Melanoides tuberculata, present in tropical fresh waters of most of the Old World before 1950, has now invaded the Neotropical area. The phylogeography of this snail was studied to evaluate the pathways and number of such invasions. Because of parthenogenetic reproduction, individuals are structured into genetical clones. Within populations from both the original and invaded areas, several morphologically distinct clones (referred to as morphs) often coexist but the amount of genetic divergence among morphs is unknown. Individuals from 27 morphs and 40 populations world-wide were sequenced at two mitochondrial genes (12S and 16S). Our phylogenetic reconstruction suggests that (i) most of the morphological variation observed in the New World predates invasion, (ii) at least six independent introductions have occurred, and (iii) invasive clones are found throughout most of the phylogenetic tree and do not come from a particular region of the area of origin. Two ideas are discussed in the light of these results. The first lies with the specificities of parthenogenesis in an invasion context. While in sexual species, independently introduced populations eventually merge into a single invasive population, in a parthenogenetic species independently introduced clones have distinct invasion dynamics and possibly exclude each other. Second, although repeated invasions in Melanoides may have an impact on indigenous molluscan faunas, their most likely effect is the world-wide homogenization of the invasive taxon itself.     

Comparative phylogeography and the history of endemic vertebrates in the Wet Tropics rainforests of Australia

We examine the effects of historical climate change on vertebrate differentiation in tropical rainforest by comparing phylogeographic patterns in six species of widespread rainforest-restricted herpetofauna from throughout the Wet Tropics of Australia. Qualitative and quantitative comparisons of phylogeographic structure reveal strikingly similar patterns of pre-Pleistocene vicariant population differentiation on either side of a previously identified biogeographic break (variously referred to as the Black Mountain Barrier or Corridor; BMC). While divergence across the BMC antedates the Pleistocene, the impact of Quaternary climate change is apparent in populations on either side of the BMC. Consistent with palaeoclimatological reconstructions for the region, the distribution and degree of mtDNA diversity suggests that populations were fragmented and reduced to multiple refugia during Pleistocene glacial periods, with expansion following Holocene rainforest recovery. This pattern is repeated on both sides of the BMC, but substantial differences in the amount and distribution of mtDNA diversity within species indicate the importance of species-specific ecological characteristics. The historical processes of extinction and (re)colonization revealed by the comparative phylogeographic analysis of mtDNA sequences substantiate earlier suggestions that current regional patterns of species distribution and diversity in the Wet Tropics are largely determined by local extinctions and subsequent recolonization driven by Quaternary climate changes.     

Comparative phylogeography of eastern chipmunks and white-footed mice in relation to the individualistic nature of species

Palaeoecological studies have demonstrated that ecological communities as a whole did not remain stable throughout the climatic fluctuations of the Quaternary. The result is that long-term associations of species cannot be inferred by contemporary associations in ecological communities. Therefore, the evolutionary significance of any contemporary ecological interactions among species and of the biotic community within which species have evolved also cannot be assumed from contemporary conditions. Comparative phylogeographic data provide a method to identify species within ecological communities that have shared biogeographic histories. We present an example of a long-term association between populations of two mammalian species, eastern chipmunks (Tamias striatus) and white-footed mice (Peromyscus leucopus), which are commonly associated with deciduous forest habitats. The distribution of mitochondrial DNA variation in T. striatus and P. leucopus from previously glaciated regions of the eastern United States support the hypothesis that, in at least part of their range, genetic lineages of the two species have expanded from similar population sources since the Last Glacial Maximum. In addition, the spatial concordance of genetic lineages of T. striatus and P. leucopus with the oak-savannah forest formations of Wisconsin and Illinois, suggest that populations associated with this community colonized the area in association with a set of arboreal species that comprise their deciduous forest habitat.     

Comparative phylogeography reveals a shared impact of pleistocene environmental change in shaping genetic diversity within nine Anopheles mosquito species across the Indo-Burma biodiversity hotspot

South-East Asia is one of the world's richest regions in terms of biodiversity. An understanding of the distribution of diversity and the factors shaping it is lacking, yet essential for identifying conservation priorities for the region's highly threatened biodiversity. Here, we take a large-scale comparative approach, combining data from nine forest-associated Anopheles mosquito species and using statistical phylogeographical methods to disentangle the effects of environmental history, species-specific ecology and random coalescent effects. Spatially explicit modelling of Pleistocene demographic history supports a common influence of environmental events in shaping the genetic diversity of all species examined, despite differences in species' mtDNA gene trees. Populations were periodically restricted to allopatric northeastern and northwestern refugia, most likely due to Pleistocene forest fragmentation. Subsequent southwards post-glacial recolonization is supported by a north-south gradient of decreasing genetic diversity. Repeated allopatric fragmentation and recolonization have led to the formation of deeply divergent geographical lineages within four species and a suture zone where these intraspecific lineages meet along the Thai-Myanmar border. A common environmental influence for this divergence was further indicated by strong support for simultaneous divergence within the same four species, dating to approximately 900 thousand years ago (kya). Differences in the geographical structuring of genetic diversity between species are probably the result of varying species' biology. The findings have important implications for conservation planning; if the refugial regions and suture zone identified here are shared by other forest taxa, the unique and high levels of genetic diversity they house will make these areas conservation priorities.     

A climate change context for the decline of a foundation tree species in south-western Australia: insights from phylogeography and species distribution modelling

Background and Aims A worldwide increase in tree decline and mortality has been linked to climate change and, where these represent foundation species, this can have important implications for ecosystem functions. This study tests a combined approach of phylogeographic analysis and species distribution modelling to provide a climate change context for an observed decline in crown health and an increase in mortality in Eucalyptus wandoo, an endemic tree of south-western Australia.Methods Phylogeographic analyses were undertaken using restriction fragment length polymorphism analysis of chloroplast DNA in 26 populations across the species distribution. Parsimony analysis of haplotype relationships was conducted, a haplotype network was prepared, and haplotype and nucleotide diversity were calculated. Species distribution modelling was undertaken using Maxent models based on extant species occurrences and projected to climate models of the last glacial maximum (LGM).Key Results A structured pattern of diversity was identified, with the presence of two groups that followed a climatic gradient from mesic to semi-arid regions. Most populations were represented by a single haplotype, but many haplotypes were shared among populations, with some having widespread distributions. A putative refugial area with high haplotype diversity was identified at the centre of the species distribution. Species distribution modelling showed high climatic suitability at the LGM and high climatic stability in the central region where higher genetic diversity was found, and low suitability elsewhere, consistent with a pattern of range contraction.Conclusions Combination of phylogeography and paleo-distribution modelling can provide an evolutionary context for climate-driven tree decline, as both can be used to cross-validate evidence for refugia and contraction under harsh climatic conditions. This approach identified a central refugial area in the test species E. wandoo, with more recent expansion into peripheral areas from where it had contracted at the LGM. This signature of contraction from lower rainfall areas is consistent with current observations of decline on the semi-arid margin of the range, and indicates low capacity to tolerate forecast climatic change. Identification of a paleo-historical context for current tree decline enables conservation interventions to focus on maintaining genetic diversity, which provides the evolutionary potential for adaptation to climate change.     

A multilocus study of pine grosbeak phylogeography supports the pattern of greater intercontinental divergence in Holarctic boreal forest birds than in birds inhabiting other high-latitude habitats

Aim Boreal forest bird species appear to be divided into lineages endemic to each northern continent, in contrast to Holarctic species living in open habitats. For example, the three-toed woodpecker (Picoides tridactylus) and the winter wren (Troglodytes troglodytes) have divergent Nearctic and Palaearctic mitochondrial DNA clades. Furthermore, in these species, the next closest relative of the Nearctic/Palaearctic sister lineages is the Nearctic clade, suggesting that the Palaearctic may have been colonized from the Nearctic. The aim of this study is to test this pattern of intercontinental divergence and colonization in another Holarctic boreal forest resident – the pine grosbeak (Pinicola enucleator). Location The Holarctic. Methods We sequenced the mitochondrial ND2 gene and Z-specific intron 9 of the ACO1 gene for 74 pine grosbeaks collected across the Holarctic. The sequences were used to reconstruct the phylogeographical history of this species using maximum likelihood analysis. Results We discovered two distinct mitochondrial and Z-specific lineages in the Nearctic and one in the Palaearctic. The two Nearctic mtDNA lineages, one in the northern boreal forest and one in south-western mountain forest, were more closely related to each other than either was to the Palaearctic clade. Two Nearctic Z-chromosome clades were sympatric in the boreal and south-western mountain forests. Unlike the topology of the mtDNA tree, the relationship among the Z-chromosome clades was the same as in the three-toed woodpecker and winter wren [Nearctic (Nearctic, Palaearctic)]. The Palaearctic Z-chromosome clade had much lower genetic diversity and a single-peak mismatch distribution with a mean < 25% of that for either Nearctic region, both of which had ragged mismatch distributions. Main conclusions Our data suggest that, similar to the other boreal forest species, the pine grosbeak has divergent lineages in each northern continent and could have colonized the Palaearctic from the Nearctic. Compared with many Holarctic birds inhabiting open habitats, boreal forest species appear to be more differentiated, possibly because the boreal forests of the Nearctic and Palaearctic have been isolated since the Pliocene (3.5 Ma).     

Intraspecific phylogeography in the sedge frog Litoria fallax (Hylidae) indicates pre-Pleistocene vicariance of an open forest species from eastern Australia

The eastern sedge frog Litoria fallax (Anura: Hylidae) is common throughout the open forests and coastal wetlands along the eastern coast of Australia. Its range spans four biogeographical zones from northern Queensland to central New South Wales. Phylogenetic analysis of mitochondrial DNA (mtDNA) haplotypes of 87 L. fallax individuals from 22 populations identified two major mtDNA lineages, differing by 11-12% sequence divergence. The two clades of haplotypes were separated by the McPherson Range, indicating that this mesic upland area has acted as a major long-term barrier to gene flow for this open forest species. Slight isolation by distance was observed within both the northern and southern lineages but was insufficient to explain the large sequence divergence between lineages. Within the northern lineage, additional phylogeographical structure was observed across the relatively dry Burdekin Gap which separates Atherton populations from all populations in the central and eastern Queensland biogeographical zones. There was less phylogeographical structure in the southern lineage suggesting historical gene flow across the drier portions of the Great Dividing Range. These data, together with recent observations of deep phylogeographical divergences in rainforest-restricted Litoria suggest that the east coast hylids of Australia represent an old (Tertiary) radiation. Individual species of Litoria have been strongly affected by climatic and ecological barriers to gene flow during the Quaternary.     

A mitochondrial phylogeography of Brachidontes variabilis (Bivalvia: Mytilidae) reveals three cryptic species

This study examined genetic variation across the range of Brachidontes variabilis to produce a molecular phylogeography. Neighbour joining (NJ), minimum evolution (ME) and maximum parsimony (MP) trees based on partial mitochondrial DNA sequences of 16S-rDNA and cytochrome oxidase (COI) genes revealed three monophyletic clades: (1) Brachidontes pharaonis s.l. from the Mediterranean Sea and the Red Sea; (2) B. variabilis from the Indian Ocean; (3) B. variabilis from the western Pacific Ocean. Although the three clades have never been differentiated by malacologists employing conventional morphological keys, they should be ascribed to the taxonomic rank of species. The nucleotide divergences between Brachidontes lineages (between 10.3% and 23.2%) were substantially higher than the divergence between congeneric Mytilus species (2.3–6.7%) and corresponded to interspecific divergences found in other bivalvia, indicating that they should be considered three different species. Analysis of the 16S-rDNA sequences revealed heteroplasmy, indicating dual uniparental inheritance (DUI) of mtDNA in the species of Brachidontes collected in the Indian Ocean, but not in the species in the Pacific nor in the species in the Red Sea and the Mediterranean Sea. When we employed the conventional estimate of the rate of mitochondrial sequence divergence (2% per million years), the divergence times for the three monophyletic lineages were 6–11 Myr for the Indian Ocean and Pacific Ocean Brachidontes sp. and 6.5–9 Myr for the Red Sea and Indian Ocean Brachidontes sp . Thus, these species diverged from one another during the Miocene (23.8–5.3 Myr). We infer that a common ancestor of the three Brachidontes species probably had an Indo-Pacific distribution and that vicariance events, linked to Pleistocene glaciations first and then to the opening of the Red Sea, produced three monophyletic lineages.     

Statistical phylogeography: methods of evaluating and minimizing inference errors

Nested clade phylogeographical analysis (NCPA) has become a common tool in intraspecific phylogeography. To evaluate the validity of its inferences, NCPA was applied to actual data sets with 150 strong a priori expectations, the majority of which had not been analysed previously by NCPA. NCPA did well overall, but it sometimes failed to detect an expected event and less commonly resulted in a false positive. An examination of these errors suggested some alterations in the NCPA inference key, and these modifications reduce the incidence of false positives at the cost of a slight reduction in power. Moreover, NCPA does equally well in inferring events regardless of the presence or absence of other, unrelated events. A reanalysis of some recent computer simulations that are seemingly discordant with these results revealed that NCPA performed appropriately in these simulated samples and was not prone to a high rate of false positives under sampling assumptions that typify real data sets. NCPA makes a posteriori use of an explicit inference key for biological interpretation after statistical hypothesis testing. Alternatives to NCPA that claim that biological inference emerges directly from statistical testing are shown in fact to use an a priori inference key, albeit implicitly. It is argued that the a priori and a posteriori approaches to intraspecific phylogeography are complementary, not contradictory. Finally, cross-validation using multiple DNA regions is shown to be a powerful method of minimizing inference errors. A likelihood ratio hypothesis testing framework has been developed that allows testing of phylogeographical hypotheses, extends NCPA to testing specific hypotheses not within the formal inference key (such as the out-of-Africa replacement hypothesis of recent human evolution) and integrates intra- and interspecific phylogeographical inference.