Phylogeographical structure and regional history of the dusky-footed woodrat, Neotoma fuscipes

The dusky-footed woodrat, Neotoma fuscipes, is a medium-sized rodent that inhabits low elevation woodland habitats along the Pacific coast of North America from Oregon, throughout California and into Baja California. Analyses of mitochondrial sequence variation throughout the distribution reveal substantial phylogeographical structure within N. fuscipes. The major mitochondrial lineages are largely concordant with previously identified morphological subdivisions within the taxon. The geographical distribution of distinct clades suggests that a combination of topographic barriers and the expansion and contraction of suitable habitat during the past 2 million years, especially along particular mountain ranges, have played a major role in the diversification of N. fuscipes. Furthermore, relatively low levels of genetic variation across the northern half of the distribution suggest that dusky-footed woodrats may have only recently expanded into this region.     

Validating the use of woodrat (Neotoma) middens for documenting natural invasions

Aim Plant macrofossils in fossil woodrat (Neotoma) middens are the primary source of information on late Quaternary biogeographical history of plants in arid and semi‐arid regions of North America. Macrofossil records from middens are playing particularly important roles in documenting spatial and temporal patterns of plant migrations and invasions since the last glacial maximum 21,000 years ago. However, relatively few actualistic studies comparing contents of modern middens with surrounding flora and vegetation have been carried out. The primary aim of this study is to assess the reliability of midden assemblages in detecting the presence of tree, shrub and several other plant species growing on the surrounding landscape. The secondary aims are to determine whether probability of occurrence of species in middens is related to abundance in vegetation, and whether representation of individual species in middens is contingent on presence/absence or abundance of other species. Location Our five study sites were bedrock escarpments or canyons in the central Rocky Mountains (north‐eastern Utah, central Wyoming and south‐central Montana). All sites were in conifer woodland or forest/woodland variously dominated by Juniperus osteosperma, J. scopulorum, Pinus edulis, P. flexilis and Pseudotsuga menziesii. Neotoma cinerea is the only woodrat species in the region. Methods Macrofossil assemblages from 59 modern middens (all showing clear signs of recent or ongoing woodrat activity) were compared with floristic composition of vegetation within 50 m of the middens, and with percent cover of vegetation within 30 m of the middens. Results Coniferous trees and shrubs were well‐represented in middens, occurring consistently even when abundance in the local vegetation was very low. Juniperus osteosperma and J. scopulorum were particularly well‐represented, occurring in middens regardless of local abundance. Other conifers (P. edulis, P. flexilis, P. ponderosa, Pseudotsuga menziesii) were occasionally absent from middens when abundance in vegetation was low (< 20% canopy cover). Occurrence of dicot shrubs and graminoids was less consistent. Main conclusions Middens constructed by N. cinerea are highly reliable sensors of presence/absence of J. osteosperma and J. scopulorum, and hence can be used to infer invasions and past biogeographical distributions of these species. The middens are also reliable in registering populations of other conifers, although presence in middens may be contingent on local abundance. Additional comparative studies are needed to develop a sound empirical basis for using middens of N. cinerea and other species to infer past presence/absence of plant species on the landscape, and to explore the vegetation‐sensing properties of midden assemblages.     

Predicting woodrat (Neotoma) responses to anthropogenic warming from studies of the palaeomidden record

Aim The influence of anthropogenic climate change on organisms is an area of great scientific concern. Increasingly there is recognition that abrupt climate transitions have occurred over the late Quaternary; studies of these shifts may yield insights into likely biotic responses to contemporary warming. Here, we review research undertaken over the past decade investigating the response of Neotoma (woodrats) body size and distribution to climate change over the late Quaternary (the last 40,000 years). By integrating information from woodrat palaeomiddens, historical museum specimens and field studies of modern populations, we identify potential evolutionary responses to climate change occurring over a variety of temporal and spatial scales. Specifically, we characterize climatic thresholds in the past that led to local species extirpation and/or range alterations rather than in situ adaptation, and apply them to anticipate potential biotic responses to anthropogenic climate change. Location Middens were collected at about 55 sites scattered across the western United States, ranging from about 34 to 46° N and about 104 to 116° W, respectively. Data for modern populations were drawn from studies conducted in Death Valley, California, Missoula, Montana and the Sevilleta LTER site in central New Mexico. Methods We analysed faecal pellets from midden series collected at numerous cave sites across the western United States. From these we estimated body mass using techniques validated in earlier studies. We compared body size fluctuations at different elevations in different regions and integrated these results with studies investigating temperature–body size tradeoffs in modern animals. We also quantify the rapidity of the size changes over the late Quaternary to estimate the evolutionary capacity of woodrats to deal with predicted rates of anthropogenic climate change over the next century. Results We find remarkable similarities across the geographical range to late Quaternary climate change. In the middle of the geographical range woodrats respond in accordance to Bergmann's rule: colder climatic conditions select for larger body size and warmer conditions select for smaller body size. Patterns are more complicated at range boundaries, and local environmental conditions influence the observed response. In general, woodrat body size fluctuates with approximately the same amplitude and frequency as climate; there is a significant and positive correlation between woodrat body size and generalized climate proxies (such as ice core records). Woodrats have achieved evolutionary rates of change equal to or greater than those needed to adapt in situ to anthropogenic climate change. Main conclusions In situ body size evolution is a likely outcome of climate change, and such shifts are part of a normal spectrum of adaptation. Woodrats appear to be subject to ongoing body size selection in response to fluctuating environmental conditions. Allometric considerations suggest that these shifts in body size lead to substantial changes in the physiology, life history and ecology of woodrats, and on their direct and indirect interactions with other organisms in the ecosystem. Our work highlights the importance of a finely resolved and long‐term record in understanding biotic responses to climatic shifts.     

Niche shifting in response to warming climate after the last glacial maximum: inference from genetic data and niche assessments in the chisel‐toothed kangaroo rat (Dipodomys microps)

During Pleistocene glacial‐interglacial cycles, the geographic range is often assumed to have shifted as a species tracks its climatic niche. Alternatively, the geographic range would not necessarily shift if a species can adapt in situ to a changing environment. The potential for a species to persist in place might increase with the diversity of habitat types that a species exploits. We evaluate evidence for either range shift or range stability between the last glacial maximum (LGM) and present time in the chisel‐toothed kangaroo rat (Dipodomys microps), an endemic of the Great Basin and Mojave deserts. We modeled how the species’ range would have changed if the climatic niche of the species remained conserved between the LGM and present time. The climatic models imply that if D. microps inhabited the same climatic niche during the LGM as it does today, the species would have persisted primarily within the warm Mojave Desert and expanded northwards into the cold Great Basin only after the LGM. Contrary to the climatic models, the mitochondrial DNA assessment revealed signals of population persistence within the current distribution of the species throughout at least the latest glacial‐interglacial cycle. We concluded that D. microps did not track its climatic niche during late Pleistocene oscillations, but rather met the challenge of a changing environment by shifting its niche and retaining large portions of its distribution. We speculate that this kind of response to fluctuating climate was possible because of ‘niche drifting’, an alteration of the species’ realized niche due to plasticity in various biological characters. Our study provides an example of an approach to reconstruct species’ responses to past climatic changes that can be used to evaluate whether and to what extent taxa have capacity to shift their niches in response to the changing environment – information becoming increasingly important to predicting biotic responses to future environmental changes.     

Persistence and diversification of the Holarctic shrew,Sorex tundrensis (Family Soricidae), in response to climate change

Environmental processes govern demography, species movements, community turnover and diversification and yet in many respects these dynamics are still poorly understood at high latitudes. We investigate the combined effects of climate change and geography through time for a widespread Holarctic shrew, Sorex tundrensis. We include a comprehensive suite of closely related outgroup taxa and three independent loci to explore phylogeographic structure and historical demography. We then explore the implications of these findings for other members of boreal communities. The tundra shrew and its sister species, the Tien Shan shrew (Sorex asper), exhibit strong geographic population structure across Siberia and into Beringia illustrating local centres of endemism that correspond to Late Pleistocene refugia. Ecological niche predictions for both current and historical distributions indicate a model of persistence through time despite dramatic climate change. Species tree estimation under a coalescent process suggests that isolation between populations has been maintained across timeframes deeper than the periodicity of Pleistocene glacial cycling. That some species such as the tundra shrew have a history of persistence largely independent of changing climate, whereas other boreal species shifted their ranges in response to climate change, highlights the dynamic processes of community assembly at high latitudes.     

Phylogeography of the mountain chickadee (Poecile gambeli): diversification, introgression, and expansion in response to Quaternary climate change

Since the late 1990s, molecular techniques have fuelled debate about the role of Pleistocene glacial cycles in structuring contemporary avian diversity in North America. The debate is still heated; however, there is widespread agreement that the Pleistocene glacial cycles forced the repeated contraction, fragmentation, and expansion of the North American biota. These demographic processes should leave genetic 'footprints' in modern descendants, suggesting that detailed population genetic studies of contemporary species provide the key to elucidating the impact of the late Quaternary (late Pleistocene-Holocene). We present an analysis of mitochondrial DNA (mtDNA) variation in the mountain chickadee (Poecile gambeli) in an attempt to examine the genetic evidence of the impact of the late Quaternary glacial cycles. Phylogenetic analyses reveal two strongly supported clades of P. gambeli: an Eastern Clade (Rocky Mountains and Great Basin) and a Western Clade (Sierra Nevada and Cascades). Post-glacial introgression is apparent between these two clades in the Mono Lake region of Central California. Within the Eastern Clade there is evidence of isolation-by-distance in the Rocky Mountain populations, and of limited gene flow into and around the Great Basin. Coalescent analysis of genetic variation in the Western Clade indicates that northern (Sierra Nevada/Cascades) and southern (Transverse/Peninsular Ranges) populations have been isolated and evolving independently for nearly 60,000 years.     

Are large‐scale distributional shifts of the blue‐winged macaw (Primolius maracana) related to climate change?

Aim To evaluate whether observed geographical shifts in the distribution of the blue‐winged macaw (Primolius maracana) are related to ongoing processes of global climate change. This species is vulnerable to extinction and has shown striking range retractions in recent decades, withdrawing broadly from southern portions of its historical distribution. Its range reduction has generally been attributed to the effects of habitat loss; however, as this species has also disappeared from large forested areas, consideration of other factors that may act in concert is merited. Location Historical distribution of the blue‐winged macaw in Brazil, eastern Paraguay and northern Argentina. Methods We used a correlative approach to test a hypothesis of causation of observed shifts by reduction of habitable areas mediated by climate change. We developed models of the ecological niche requirements of the blue‐winged macaw, based on point‐occurrence data and climate scenarios for pre‐1950 and post‐1950 periods, and tested model predictivity for anticipating geographical distributions within time periods. Then we projected each model to the other time period and compared distributions predicted under both climate scenarios to assess shifts of habitable areas across decades and to evaluate an explanation for observed range retractions. Results Differences between predicted distributions of the blue‐winged macaw over the twentieth century were, in general, minor and no change in suitability of landscapes was predicted across large areas of the species’ original range in different time periods. No tendency towards range retraction in the south was predicted, rather conditions in the southern part of the species’ range tended to show improvement for the species. Main conclusions Our test permitted elimination of climate change as a likely explanation for the observed shifts in the distribution of the blue‐winged macaw, and points rather to other causal explanations (e.g. changing regional land use, emerging diseases).     

Mitochondrial DNA phylogeography in northern grasshopper mice (Onychomys leucogaster) — the influence of Quaternary climatic oscillations on population dispersion and divergence

The details of mitochondrial DNA (mtDNA) phylogenetic structure of the northern grasshopper mouse Onychomys leucogaster were examined using populations from a postulated area of endemism that includes three arid regions (Colorado Plateaus, Interior Plains, and Wyoming Basins) in western North America. Fifteen tetra- and heptanucleotide restriction enzymes were used to assay restriction-site variation in a 2150-bp PCR-amplified fragment of mtDNA representing the ND2 and part of the COI gene regions. A total of 18 mtDNA haplotypes were detected. Although overall genetic divergence among these haplotypes was low (average = 1.1%), phylogeographic structuring was apparent. Notably, a clear phylogenetic split separated one group of haplotypes restricted to the Wyoming Basins from all others. This phylogenetic split was further corroborated by examination of nucleotide sequence variation from a 270-bp stretch of the mtDNA cytochrome b gene. Overall geographic and phylogenetic patterns suggest a complex history of geographic structuring and subsequent mixing of populations of grasshopper mice throughout the late Pleistocene. These patterns of variation are evaluated relative to alternative hypotheses about biotic responses to Quaternary climatic oscillations in western North American arid regions.     

Phylogeography of the Western Lyresnake (Trimorphodon biscutatus): testing aridland biogeographical hypotheses across the Nearctic-Neotropical transition

The Western Lyresnake (Trimorphodon biscutatus) is a widespread, polytypic taxon inhabiting arid regions from the warm deserts of the southwestern United States southward along the Pacific versant of Mexico to the tropical deciduous forests of Mesoamerica. This broadly distributed species provides a unique opportunity to evaluate a priori biogeographical hypotheses spanning two major distinct biogeographical realms (the Nearctic and Neotropical) that are usually treated separately in phylogeographical analyses. I investigated the phylogeography of T. biscutatus using maximum likelihood and Bayesian phylogenetic analysis of mitochondrial DNA (mtDNA) from across this species' range. Phylogenetic analyses recovered five well-supported clades whose boundaries are concordant with existing geographical barriers, a pattern consistent with a model of vicariant allopatric divergence. Assuming a vicariance model, divergence times between mitochondrial lineages were estimated using Bayesian relaxed molecular clock methods calibrated using geological information from putative vicariant events. Divergence time point estimates were bounded by broad confidence intervals, and thus these highly conservative estimates should be considered tentative hypotheses at best. Comparison of mtDNA lineages and taxa traditionally recognized as subspecies based on morphology suggest this taxon is comprised of multiple independent lineages at various stages of divergence, ranging from putative secondary contact and hybridization to sympatry of 'subspecies'.     

Influence of late Quaternary climate change on present patterns of genetic variation in valley oak,Quercus lobata Née

Phylogeography and ecological niche models (ENMs) suggest that late Quaternary glacial cycles have played a prominent role in shaping present population genetic structure and diversity, but have not applied quantitative methods to dissect the relative contribution of past and present climate vs. other forces. We integrate multilocus phylogeography, climate‐based ENMs and multivariate statistical approaches to infer the effects of late Quaternary climate change on contemporary genetic variation of valley oak (Quercus lobata Née). ENMs indicated that valley oak maintained a stable distribution with local migration from the last interglacial period (~120 ka) to the Last Glacial Maximum (~21 ka, LGM) to the present compared with large‐scale range shifts for an eastern North American white oak (Quercus alba L.). Coast Range and Sierra Nevada foothill populations diverged in the late Pleistocene before the LGM [104 ka (28–1622)] and have occupied somewhat distinct climate niches, according to ENMs and coalescent analyses of divergence time. In accordance with neutral expectations for stable populations, nuclear microsatellite diversity positively correlated with niche stability from the LGM to present. Most strikingly, nuclear and chloroplast microsatellite variation significantly correlated with LGM climate, even after controlling for associations with geographic location and present climate using partial redundancy analyses. Variance partitioning showed that LGM climate uniquely explains a similar proportion of genetic variance as present climate (16% vs. 11–18%), and together, past and present climate explains more than geography (19%). Climate can influence local expansion–contraction dynamics, flowering phenology and thus gene flow, and/or impose selective pressures. These results highlight the lingering effect of past climate on genetic variation in species with stable distributions.     

Impact of climate change on vector transmission of Trypanosoma cruzi (Chagas, 1909) in North America

Climate change can influence the geographical range of the ecological niche of pathogens by altering biotic interactions with vectors and reservoirs. The distributions of 20 epidemiologically important triatomine species in North America were modelled, comparing the genetic algorithm for rule‐set prediction (GARP) and maximum entropy (MaxEnt), with or without topographical variables. Potential shifts in transmission niche for Trypanosoma cruzi (Trypanosomatida: Trypanosomatidae) (Chagas, 1909) were analysed for 2050 and 2070 in Representative Concentration Pathway (RCP) 4.5 and RCP 8.5. There were no significant quantitative range differences between the GARP and MaxEnt models, but GARP models best represented known distributions for most species [partial‐receiver operating characteristic (ROC) > 1]; elevation was an important variable contributing to the ecological niche model (ENM). There was little difference between niche breadth projections for RCP 4.5 and RCP 8.5; the majority of species shifted significantly in both periods. Those species with the greatest current distribution range are expected to have the greatest shifts. Positional changes in the centroid, although reduced for most species, were associated with latitude. A significant increase or decrease in mean niche elevation is expected principally for Neotropical 1 species. The impact of climate change will be specific to each species, its biogeographical region and its latitude. North American triatomines with the greatest current distribution ranges (Nearctic 2 and Nearctic/Neotropical) will have the greatest future distribution shifts. Significant shifts (increases or decreases) in mean elevation over time are projected principally for the Neotropical species with the broadest current distributions. Changes in the vector exposure threat to the human population were significant for both future periods, with a 1.48% increase for urban populations and a 1.76% increase for rural populations in 2050.     

Extensive population expansion of Pedicularis longiflora (Orobanchaceae) on the Qinghai‐Tibetan Plateau and its correlation with the Quaternary climate change

The Qinghai‐Tibetan Plateau (QTP) is thought to be more strongly affected by the Quaternary glaciations than most other regions of the same latitude. It would be of great interest to investigate the population genetic structure of organisms distributed on the platform and its correlation with the Quaternary climatic oscillations. Here we used the chloroplast (cp)DNA trnT‐trnF sequence to study genetic variation and phylogeography of Pedicularis longiflora, an alpine herb with extensive distribution on the QTP. Based on a range‐wide sampling comprising 41 populations and 910 individuals, we detected 30 cpDNA haplotypes that were divided into five clades by phylogenetic and network analyses and a strong phylogeographical structure. All haplotypes but one in the three basal clades occur exclusively in the southeast QTP, whereas haplotypes in the young clade V occupy almost the whole species range. In particular, the young haplotype H18 occurs in 420 individuals, even at a frequency of 100% in some QTP platform populations and the Altai population. The haplotype distribution pattern, together with molecular clock estimation and mismatch distribution analysis, suggests that the southeast QTP was either a refuge for P. longiflora during the Quaternary climatic change or is the place of origin of the species. The present wide distribution of the species on the QTP platform has resulted from recent population expansions which could be dated back to 120 000–17 000 years ago, a period mostly before the last glacial maximum. The possible relationships among geographic genetic structure, climatic change and species diversification in Pedicularis are also discussed.     

Ecological niche modelling of montane mammals in the Great Basin, North America: examining past and present connectivity of species across basins and ranges

Aim The goal of this study was to determine the extent of suitable habitats across the basins and ranges of the Great Basin for 13 montane mammals in the present and during the Last Glacial Maximum (LGM). For all these mammal species, we test whether: (1) more suitable habitat was available in basin areas during the LGM; (2) suitable habitat shifted upwards in elevation between the LGM and the present; (3) more ranges have suitable habitat than are currently occupied; and (4) these species are currently restricted to suitable habitats at higher‐elevation range areas. We also examine whether and how much distributional response varies among these montane mammal species. Location The Great Basin of western North America. Methods We re‐examine the past and present distributions of 13 Great Basin montane mammals using ecological niche modelling techniques that utilize now widely available species occurrence data and new, fine‐scale past climatological GIS layers in the present and at the LGM. These methods provide an objective, repeatable means for visual comparison of past and present modelled distributions for species examined in previous biogeographical studies. Results Our results indicate greater areal and lower elevational suitable habitat in the LGM than at present for nearly all montane mammals, and that there is more suitable habitat at present than is currently occupied. Our results also show that lowland areas provide suitable dispersal routes between ranges for most of the montane mammals both at the LGM and at present. However, three of the 13 species have little to no predicted suitable habitat in the LGM near currently occupied ranges, in contrast to the pattern for the other 10. For these species, the model results support more recent long‐distance colonization. Main conclusions Our finding of suitable lowland dispersal routes in the present for most species supports and greatly extends similar findings from single‐species studies. Our results also provide a visually striking confirmation that changes in species distribution and colonization histories of Great Basin montane mammals vary in a fashion related to the tolerances and requirements of each of these species; this has previously been hypothesized but not rigorously tested for multiple montane mammals in the region.     

A phylogeographic analysis of populations of the wood turtle (Glyptemys insculpta) throughout its range

We investigated the phylogeography of wood turtles, Glyptemys insculpta, in North America using 750 bp of the mitochondrial control region from 117 individuals sampled at 29 localities across the species' range. A total of 21 haplotypes were identified and little genetic variation was found. The highest pairwise difference was 2%. From nested clade analysis (NCA), one main postglacial dispersal route was inferred along the east coast, with subsequent westward dispersal. NCA further revealed some patterns of restricted gene flow/dispersal. We propose that wood turtles experienced a combined effect of bottleneck during the Pleistocene as well as of selective sweep, which produced the low level of variation observed. Following the Pleistocene, wood turtles would have undergone a rapid northward expansion from a common southern refugium as glaciers retreated. These findings shed light on where to direct conservation priorities, on conservation strategies needed, and on the potential effects of interpopulation transfers for this vulnerable species.     

Relative roles of Neogene vicariance and Quaternary climate change on the historical diversification of bunchgrass lizards (Sceloporus scalaris group) in Mexico

Neogene vicariance during the Miocene and Pliocene and Quaternary climate change have synergistically driven diversification in Mexican highland taxa. We investigated the impacts of these processes on genetic diversification in the widely distributed bunchgrass lizards in the Sceloporus scalaris group. We searched for correlations between timing in diversification and timing of (1) a period of marked volcanism across the Trans-Mexican Volcanic Belt in central Mexico 3-7.5 million years ago (Ma) and (2) a transition to larger glacial-interglacial cycles during the mid-Pleistocene. From our phylogenetic analyses of mitochondrial DNA we identified two major clades that contained 13 strongly supported lineages. One clade contained lineages from the two northern sierras of Mexico, and the other clade included lineages associated with the Trans-Mexican Volcanic Belt and Central Mexican Plateau. Results provided support for Neogene divergences within the S. scalaris group in response to uplift of the Trans-Mexican Volcanic Belt, a pattern observed in several co-distributed taxa, and suggested that Quaternary climate change likely had little effect on diversification between lineages. Uplift of the Trans-Mexican Volcanic Belt during specific time periods appears to have strongly impacted diversification in Mexican highland taxa.     

Climate change and evolution of the New World pitviper genus Agkistrodon (Viperidae)

Aim We derived phylogenies, phylogeographies, and population demographies for two North American pitvipers, Agkistrodon contortrix (Linnaeus, 1766) and A. piscivorus (Lacépède, 1789) (Viperidae: Crotalinae), as a mechanism to evaluate the impact of rapid climatic change on these taxa. Location Midwestern and eastern North America. Methods We reconstructed maximum parsimony (MP) and maximum likelihood (ML) relationships based on 846 base pairs of mitochondrial DNA (mtDNA) ATPase 8 and ATPase 6 genes sequenced over 178 individuals. We quantified range expansions, demographic histories, divergence dates and potential size differences among clades since their last period of rapid expansion. We used the Shimodaira–Hasegawa (SH) test to compare our ML tree against three biogeographical hypotheses. Results A significant SH test supported diversification of A. contortrix from northeastern Mexico into midwestern–eastern North America, where its trajectory was sundered by two vicariant events. The first (c. 5.1 Ma) segregated clades at 3.1% sequence divergence (SD) along a continental east–west moisture gradient. The second (c. 1.4 Ma) segregated clades at 2.4% SD along the Mississippi River, coincident with the formation of the modern Ohio River as a major meltwater tributary. A single glacial refugium was detected within the Apalachicola region of southeastern North America. Significant support was also found for a hypothesis of trans‐Gulf rafting by the common ancestor of A. piscivorus from eastern Mexico (possibly the Yucatan Peninsula) to northern Florida. There, a Mid–Late Pliocene marine transgression separated it at 4.8% SD from mainland North America. Significant range expansions followed compressive glacial effects in three (of four) A. contortrix clades and in two (of three) A. piscivorus clades, with the Florida A. piscivorus clade exhibiting significant distributional stasis. Main conclusions Pliocene glaciations, rapidly developing western aridity, and Pleistocene glacial meltwaters seemingly led to the diversification of A. contortrix and A. piscivorus in North America. Both species were pushed southwards by Pleistocene climate change, with subsequent northward expansions uninhibited topographically. The subspecific taxonomy used for A. contortrix and A. piscivorus today, however, appear non‐representative. The monophyletic Florida subspecies of A. piscivorus may be a distinct species (at 4.8% SD), whereas two western subspecies of A. contortrix also appear to constitute a single distinct species, pending additional analyses. We conclude that both species of Agkistrodon can be used as suitable ectothermic models to gauge impacts of future climate change.