Integrating Earth-life systems: a geogenomic approach.

For centuries, scientists have recognized and worked to understand how Earth's mutable landscape and climate shape the distribution and evolution of species. Here, we describe the emerging field of geogenomics, which uses the reciprocal and deep integration of geologic, climatic, and population genomic data to define and test cause-effect relationships between Earth and life at intermediate spatial and temporal scales (i.e., the mesoscale). Technological advances now power the detailed reconstruction of landscape and evolutionary histories, but transdisciplinary collaborations and new quantitative tools are needed to better integrate Earth-life data. Geogenomics can help build a more unified theory and characterize the boundary conditions under which geologic and climatic processes generate new biodiversity, how species' responses differ, and why.

Biodiversity and Topographic Complexity: Modern and Geohistorical Perspectives.

Topographically complex regions on land and in the oceans feature hotspots of biodiversity that reflect geological influences on ecological and evolutionary processes. Over geologic time, topographic diversity gradients wax and wane over millions of years, tracking tectonic or climatic history. Topographic diversity gradients from the present day and the past can result from the generation of species by vicariance or from the accumulation of species from dispersal into a region with strong environmental gradients. Biological and geological approaches must be integrated to test alternative models of diversification along topographic gradients. Reciprocal illumination among phylogenetic, phylogeographic, ecological, paleontological, tectonic, and climatic perspectives is an emerging frontier of biogeographic research.

Comparative phylogeography clarifies the complexity and problems of continental distribution that drove A. R. Wallace to favor islands.

Deciphering the geographic context of diversification and distributional dynamics in continental biotas has long been an interest of biogeographers, ecologists, and evolutionary biologists. Thirty years ago, the approach now known as comparative phylogeography was introduced in a landmark study of a continental biota. Here, I use a set of 455 studies to explore the current scope of continental comparative phylogeography, including geographic, conceptual, temporal, ecological, and genomic attributes. Geographically, studies are more frequent in the northern hemisphere, but the south is catching up. Most studies focus on a Quaternary timeframe, but the Neogene is well represented. As such, explanations for geographic structure and history include geological and climatic events in Earth history, and responses include vicariance, dispersal, and range contraction-expansion into and out of refugia. Focal taxa are biased toward terrestrial or semiterrestrial vertebrates, although plants and invertebrates are well represented in some regions. The use of various kinds of nuclear DNA markers is increasing, as are multiple locus studies, but use of organelle DNA is not decreasing. Species distribution models are not yet widely incorporated into studies. In the future, continental comparative phylogeographers will continue to contribute to erosion of the simple vicariance vs. dispersal paradigm, including exposure of the widespread nature of temporal pseudocongruence and its implications for models of diversification; provide new templates for addressing a variety of ecological and evolutionary traits; and develop closer working relationships with earth scientists and biologists in a variety of disciplines.

Range and niche shifts in response to past climate change in the desert horned lizard (Phrynosoma platyrhinos).

During climate change, species are often assumed to shift their geographic distributions (geographic ranges) in order to track environmental conditions - niches - to which they are adapted. Recent work, however, suggests that the niches do not always remain conserved during climate change but shift instead, allowing populations to persist in place or expand into new areas. We assessed the extent of range and niche shifts in response to the warming climate after the Last Glacial Maximum (LGM) in the desert horned lizard (Phrynosoma platyrhinos), a species occupying the western deserts of North America. We used a phylogeographic approach with mitochondrial DNA sequences to approximate the species range during the LGM by identifying populations that exhibit a genetic signal of population stability versus those that exhibit a signal of a recent (likely post-LGM) geographic expansion. We then compared the climatic niche that the species occupies today with the niche it occupied during the LGM using two models of simulated LGM climate. The genetic analyses indicated that P. platyrhinos persisted within the southern Mojave and Sonoran deserts throughout the latest glacial period and expanded from these deserts northwards, into the western and eastern Great Basin, after the LGM. The climatic niche comparisons revealed that P. platyrhinos expanded its climatic niche after the LGM towards novel, warmer and drier climates that allowed it to persist within the southern deserts. Simultaneously, the species shifted its climatic niche towards greater temperature and precipitation fluctuations after the LGM. We concluded that climatic changes at the end of the LGM promoted both range and niche shifts in this lizard. The mechanism that allowed the species to shift its niche remains unknown, but phenotypic plasticity likely contributes to the species ability to adjust to climate change.

Genetic consequences of postglacial range expansion in two codistributed rodents (genus Dipodomys) depend on ecology and genetic locus.

How does range expansion affect genetic diversity in species with different ecologies, and do different types of genetic markers lead to different conclusions? We addressed these questions by assessing the genetic consequences of postglacial range expansion using mitochondrial DNA (mtDNA) and nuclear restriction site-associated DNA (RAD) sequencing in two congeneric and codistributed rodents with different ecological characteristics: the desert kangaroo rat (Dipodomys deserti), a sand specialist, and the Merriam's kangaroo rat (Dipodomys merriami), a substrate generalist. For each species, we compared genetic variation between populations that retained stable distributions throughout glacial periods and those inferred to have expanded since the last glacial maximum. Our results suggest that expanded populations of both species experienced a loss of private mtDNA haplotypes and differentiation among populations, as well as a loss of nuclear single-nucleotide polymorphism (SNP) private alleles and polymorphic loci. However, only D. deserti experienced a loss of nucleotide diversity (both mtDNA and nuclear) and nuclear heterozygosity. For all indices of diversity and differentiation that showed reduced values in the expanded areas, D. deserti populations experienced a greater degree of loss than did D. merriami populations. Additionally, patterns of loss in genetic diversity in expanded populations were substantially less extreme (by two orders of magnitude in some cases) for nuclear SNPs in both species compared to that observed for mitochondrial data. Our results demonstrate that ecological characteristics may play a role in determining genetic variation associated with range expansions, yet mtDNA diversity loss is not necessarily accompanied by a matched magnitude of loss in nuclear diversity.

Investigating the effects of Pleistocene events on genetic divergence within Richardsonius balteatus, a widely distributed western North American minnow.

BACKGROUND: Biogeographers seek to understand the influences of global climate shifts and geologic changes to the landscape on the ecology and evolution of organisms. Across both longer and shorter timeframes, the western North American landscape has experienced dynamic transformations related to various geologic processes and climatic oscillations, including events as recently as the Last Glacial Maximum (LGM; ~20 Ka) that have impacted the evolution of the North American biota. Redside shiner is a cyprinid species that is widely distributed throughout western North America. The species' native range includes several well-documented Pleistocene refugia. Here we use mitochondrial DNA sequence data to assess phylogeography, and to test two biogeographic hypotheses regarding post-glacial colonization by redside shiner: 1) Redside shiner entered the Bonneville Basin at the time of the Bonneville Flood (Late Pleistocene; 14.5 Ka), and 2) redside shiner colonized British Columbia post-glacially from a single refugium in the Upper Columbia River drainage. RESULTS: Genetic diversification in redside shiner began in the mid to late Pleistocene, but was not associated with LGM. Different clades of redside shiner were distributed in multiple glacial age refugia, and each clade retains a signature of population expansion, with clades having secondary contact in some areas. CONCLUSIONS: Divergence times between redside shiner populations in the Bonneville Basin and the Upper Snake/Columbia River drainage precedes the Bonneville Flood, thus it is unlikely that redside shiner invaded the Bonneville Basin during this flooding event. All but one British Columbia population of redside shiner are associated with the Upper Columbia River drainage with the lone exception being a population near the coast, suggesting that the province as a whole was colonized from multiple refugia, but the inland British Columbia redside shiner populations are affiliated with a refugium in the Upper Columbia River drainage.

Phylogeography of Beck's Desert Scorpion, Paruroctonus becki, reveals Pliocene diversification in the Eastern California Shear Zone and postglacial expansion in the Great Basin Desert.

The distribution of Beck's Desert Scorpion, Paruroctonus becki (Gertsch and Allred, 1965), spans the 'warm' Mojave Desert and the western portion of the 'cold' Great Basin Desert. We used genetic analyses and species distribution modeling to test whether P. becki persisted in the Great Basin Desert during the Last Glacial Maximum (LGM), or colonized the area as glacial conditions retreated and the climate warmed. Phylogenetic and network analyses of mitochondrial cytochrome c oxidase 1 (cox1), 16S rDNA, and nuclear internal transcribed spacer (ITS-2) DNA sequences uncovered five geographically-structured groups in P. becki with varying degrees of statistical support. Molecular clock estimates and the geographical arrangement of three of the groups suggested that Pliocene geological events in the tectonically dynamic Eastern California Shear Zone may have driven diversification by vicariance. Diversification was estimated to have continued through the Pleistocene, during which a group endemic to the western Great Basin diverged from a related group in the eastern Mojave Desert and western Colorado Plateau. Demographic and network analyses suggested that P. becki underwent a recent expansion in the Great Basin. According to a landscape interpolation of genetic distances, this expansion appears to have occurred from the northwest, implying that P. becki may have persisted in part of the Great Basin during the LGM. This prediction is supported by species distribution models which suggest that climate was unsuitable throughout most of the Great Basin during the LGM, but that small patches of suitable climate may have remained in areas of the Lahontan Trough.

As Old as the hills: montane scorpions in Southwestern North America reveal ancient associations between biotic diversification and landscape history.

BACKGROUND: The age of lineages has become a fundamental datum in studies exploring the interaction between geological transformation and biotic diversification. However, phylogeographical studies are often biased towards lineages that are younger than the geological features of the landscapes they inhabit. A temporally deeper historical biogeography framework may be required to address episodes of biotic diversification associated with geologically older landscape changes. Signatures of such associations may be retained in the genomes of ecologically specialized (stenotopic) taxa with limited vagility. In the study presented here, genetic data from montane scorpions in the Vaejovis vorhiesi group, restricted to humid rocky habitats in mountains across southwestern North America, were used to explore the relationship between scorpion diversification and regional geological history. RESULTS: Strong phylogeographical signal was evident within the vorhiesi group, with 27 geographically cohesive lineages inferred from a mitochondrial phylogeny. A time-calibrated multilocus species tree revealed a pattern of Miocene and Pliocene (the Neogene period) lineage diversification. An estimated 21 out of 26 cladogenetic events probably occurred prior to the onset of the Pleistocene, 2.6 million years ago. The best-fit density-dependent model suggested diversification rate in the vorhiesi group gradually decreased through time. CONCLUSIONS: Scorpions of the vorhiesi group have had a long history in the highlands of southwestern North America. Diversification among these stenotopic scorpions appears to have occurred almost entirely within the Neogene period, and is temporally consistent with the dynamic geological history of the Basin and Range, and Colorado Plateau physiographical provinces. The persistence of separate lineages at small spatial scales suggests that a combination of ecological stenotopy and limited vagility may make these scorpions particularly valuable indicators of geomorphological evolution.

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 3-7.5million 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.

Diversification in the Mexican horned lizard Phrynosoma orbiculare across a dynamic landscape.

The widespread montane Mexican horned lizard Phrynosoma orbiculare (Squamata: Phrynosomatidae) represents an ideal species to investigate the relative impacts of Neogene vicariance and Quaternary climate change on lineage diversification across the Mexican highlands. We used mitochondrial DNA to examine the maternal history of P. orbiculare and estimate the timing and tempo of lineage diversification. Based on our results, we inferred 11 geographically structured, well supported mitochondrial lineages within this species, suggesting P. orbiculare represents a species complex. Six divergences between lineages likely occurred during the Late Miocene and Pliocene, and four splits probably happened during the Pleistocene. Diversification rate appeared relatively constant through time. Spatial and temporal divergences between lineages of P. orbiculare and co-distributed taxa suggest that a distinct period of uplifting of the Transvolcanic Belt around 7.5-3 million years ago broadly impacted diversification in taxa associated with this mountain range. To the north, several river drainages acting as filter barriers differentially subdivided co-distributed highland taxa through time. Diversification patterns observed in P. orbiculare provide additional insight into the mechanisms that impacted differentiation of highland taxa across the complex Mexican highlands.

Elucidation of cryptic diversity in a widespread nearctic treefrog reveals episodes of mitochondrial gene capture as frogs diversified across a dynamic landscape.

We investigate the evolutionary history of the wide-ranging Nearctic treefrog Hyla arenicolor through the integration of extensive range-wide sampling, phylogenetic analyses of multilocus genetic data, and divergence dating. Previous phylogeographic studies of this frog documented a potential signature of introgressive hybridization from an ecologically and morphologically divergent sister species. Based on our Bayesian phylogenetic analyses of mitochondrial DNA, we inferred strong phylogeographic structure in H. arenicolor as indicated by seven well-supported clades, five of which correspond to well-defined biogeographic regions. Clades from the Balsas Basin and southwestern Central Mexican Plateau in Mexico, and the Grand Canyon of Arizona, group with the morphologically, behaviorally, and ecologically divergent mountain treefrogs in the H. eximia group, rendering H. arenicolor as paraphyletic. The phylogenetic position of at least two of these three H. arenicolor clades within the H. eximia group, however, is most likely the result of several episodes of introgressive hybridization and subsequent mitochondrial gene capture separated in time and space, as supported by evidence from the nuclear genes. Hyla arenicolor from the Balsas Basin appear to be deeply divergent from other H. arenicolor and represent a distinctly different species. Results suggests that introgressive hybridization events, both ancient and contemporary, coupled with late Neogene vicariance and Pleistocene climate-driven range shifts, have all played a role in the historical diversification of H. arenicolor.

Phylogenetic relationships of the western North American cyprinid genus Richardsonius, with an overview of phylogeographic structure.

Diversification of many North American taxa, including freshwater fishes, has been heavily influenced by the effects of complex geological and climatic events throughout the Cenozoic that have significantly altered the landscape. Here, we employ an array of phylogenetic analyses using a multiple gene tree approach to address several questions regarding the phylogenetic relationships of the North American cyprinid genus Richardsonius and two other closely related genera, Clinostomus and Iotichthys. We also use divergence time estimates generated using fossil calibrations to qualitatively assess the phylogeographic implications of evolution within the group. Mitochondrial and nuclear DNA sequences show a sister relationship between Iotichthys and Richardsonius, with Clinostomus being sister to an Iotichthys-Richardsonius clade, hence the currently recognized sister relationship between Clinostomus and Richardsonius is not supported. These genera appear to be monophyletic lineages, and sister species within genera appear to be reciprocally monophyletic. The two species within the genus Richardsonius both exhibit phylogeographic structure that is worthy of further investigation. Divergence time estimates between genera and species are Miocene or Pliocene in age, and divergence between phylogroups within species occurred in the late Pliocene to Pleistocene. These splits coincide with documented geological and climatic events.

Mitochondrial introgression and incomplete lineage sorting through space and time: phylogenetics of crotaphytid lizards.

We investigate the roles of mitochondrial introgression and incomplete lineage sorting during the phylogenetic history of crotaphytid lizards. Our Bayesian phylogenetic estimate for Crotaphytidae is based on analysis of mitochondrial DNA sequence data for 408 individuals representing the 12 extant species of Crotaphytus and Gambelia. The mitochondrial phylogeny disagrees in several respects with a previously published morphological tree, as well as with conventional species designations, and we conclude that some of this disagreement stems from hybridization-mediated mitochondrial introgression, as well as from incomplete lineage sorting. Unidirectional introgression of Crotaphytus collaris (western collared lizard) mitochondria into C. reticulatus (reticulate collared lizard) populations in the Rio Grande Valley of Texas has resulted in the replacement of ancestral C. reticulatus mitochondria over approximately two-thirds of the total range of the species, a linear distance of approximately 270 km. Introgression of C. collaris mitochondria into C. bicinctores (Great Basin collared lizard) populations in southwestern Arizona requires a more complex scenario because at least three temporally separated and superimposed introgression events appear to have occurred in this region. We propose an "introgression conveyor" model to explain this unique pattern of mitochondrial variation in this region. We show with ecological niche modeling that the predicted geographical ranges of C. collaris, C. bicinctores, and C. reticulatus during glacial maxima could have provided enhanced opportunities for past hybridization. Our analyses suggest that incomplete lineage sorting and/or introgression has further confounded the phylogenetic placements of additional species including C. nebrius, C. vestigium, C. insularis, C. grismeri, and perhaps G. copei. Despite many independent instances of interspecific hybridization among crotaphytid lizards, the species continue to maintain morphological and geographic cohesiveness throughout their ranges.

Cryptic Neogene vicariance and Quaternary dispersal of the red-spotted toad (Bufo punctatus): insights on the evolution of North American warm desert biotas.

We define the geographical distributions of mitochondrial DNA (mtDNA) lineages embedded within a broadly distributed, arid-dwelling toad, Bufo punctatus. These patterns were evaluated as they relate to hypothesized vicariant events leading to the formation of desert biotas within western North America. We assessed mtDNA sequence variation among 191 samples from 82 sites located throughout much of the species' range. Parsimony-based haplotype networks of major identified lineages were used in nested clade analysis (NCA) to further elucidate and evaluate shallow phylogeographic patterns potentially associated with Quaternary (Pleistocene-Holocene) vicariance and dispersal. Phylogenetic analyses provided strong support for three monophyletic lineages (clades) within B. punctatus. The geographical distributions of the clades showed little overlap and corresponded to the general boundaries of the Peninsular Desert, and two continental desert regions, Eastern (Chihuahuan Desert-Colorado Plateau) and Western (Mojave-Sonoran deserts), geographically separated along the Rocky Mountains and Sierra Madre Occidental. The observed divergence levels and congruence with postulated events in earth history implicate a late Neogene (latest Miocene-early Pliocene) time frame for separation of the major mtDNA lineages. Evaluation of nucleotide and haplotype diversity and interpretations from NCA reveal that populations on the Colorado Plateau resulted from a recent, likely post-Pleistocene, range expansion from the Chihuahuan Desert. Dispersal across historical barriers separating major continental clades appear to be recent, resulting in secondary contacts in at least two areas. Given the observed contact between major clades, we speculated as to why the observed deep phylogeographic structure has not been eroded during the multiple previous interglacials of the Pleistocene.

HISTORICAL BIOGEOGRAPHY IN NORTH AMERICAN ARID REGIONS: AN APPROACH USING MITOCHONDRIAL-DNA PHYLOGENY IN GRASSHOPPER MICE (GENUS ONYCHOMYS).

Restriction-endonuclease-site variation of mitochondrial DNA (mtDNA) was used to investigate patterns of geographic and phylogenetic divergence within the rodent genus Onychomys. Onychomys has occupied arid habitats in the western North American deserts, shrub-steppes, and grasslands since the late Tertiary. A phylogenetic analysis of the total mtDNA restriction-site variation throughout the range of Onychomys suggests that the distribution of this genus has been affected by the same Quaternary pluvial-interpluvial climatic fluctuations that have resulted in the periodic fragmentation of arid habitats in western North America. Onychomys mtDNA haplotypes define at least five discrete geographical subsets, suggesting that there are five areas of endemism for biota restricted to arid and semiarid habitats in North America. The mtDNA-haplotype phylogeny can be used to infer an hypothesis of historical relationships among the five areas of endemism as follows: ([{(Wyoming Basin + Interior Plains + Colorado Plateaus) + (Columbia Basin + Great Basin)} + Gulf Coastal Plain] + Chihuahuan) + Western Deserts. The results of this study point to the potential use of mtDNA-haplotype phylogenies to reconstruct historical biogeographic events in Quaternary time. The utility of mtDNA variation depends in part on the ecology and distribution of the species being examined. Therefore, our hypothesized area cladogram can be tested by investigating regional relationships in other western North American taxa with distributions similar to Onychomys.