Global determinants of insect mitochondrial genetic diversity.

Understanding global patterns of genetic diversity is essential for describing, monitoring, and preserving life on Earth. To date, efforts to map macrogenetic patterns have been restricted to vertebrates, which comprise only a small fraction of Earth's biodiversity. Here, we construct a global map of predicted insect mitochondrial genetic diversity from cytochrome c oxidase subunit 1 sequences, derived from open data. We calculate the mitochondrial genetic diversity mean and genetic diversity evenness of insect assemblages across the globe, identify their environmental correlates, and make predictions of mitochondrial genetic diversity levels in unsampled areas based on environmental data. Using a large single-locus genetic dataset of over 2 million globally distributed and georeferenced mtDNA sequences, we find that mitochondrial genetic diversity evenness follows a quadratic latitudinal gradient peaking in the subtropics. Both mitochondrial genetic diversity mean and evenness positively correlate with seasonally hot temperatures, as well as climate stability since the last glacial maximum. Our models explain 27.9% and 24.0% of the observed variation in mitochondrial genetic diversity mean and evenness in insects, respectively, making an important step towards understanding global biodiversity patterns in the most diverse animal taxon.

Human impacts outpace natural processes in the Amazon.

Amazonian environments are being degraded by modern industrial and agricultural activities at a pace far above anything previously known, imperiling its vast biodiversity reserves and globally important ecosystem services. The most substantial threats come from regional deforestation, because of export market demands, and global climate change. The Amazon is currently perched to transition rapidly from a largely forested to a nonforested landscape. These changes are happening much too rapidly for Amazonian species, peoples, and ecosystems to respond adaptively. Policies to prevent the worst outcomes are known and must be enacted immediately. We now need political will and leadership to act on this information. To fail the Amazon is to fail the biosphere, and we fail to act at our peril.

A framework for near-real time monitoring of diversity patterns based on indirect remote sensing, with an application in the Brazilian Atlantic rainforest.

Monitoring biodiversity change is key to effective conservation policy. While it is difficult to establish in situ biodiversity monitoring programs at broad geographical scales, remote sensing advances allow for near-real time Earth observations that may help with this goal. We combine periodical and freely available remote sensing information describing temperature and precipitation with curated biological information from several groups of animals and plants in the Brazilian Atlantic rainforest to design an indirect remote sensing framework that monitors potential loss and gain of biodiversity in near-real time. Using data from biological collections and information from repeated field inventories, we demonstrate that this framework has the potential to accurately predict trends of biodiversity change for both taxonomic and phylogenetic diversity. The framework identifies areas of potential diversity loss more accurately than areas of species gain, and performs best when applied to broadly distributed groups of animals and plants.

Links between prey assemblages and poison frog toxins: A landscape ecology approach to assess how biotic interactions affect species phenotypes.

Ecological studies of species pairs showed that biotic interactions promote phenotypic change and eco-evolutionary feedbacks. However, it is unclear how phenotypes respond to synergistic interactions with multiple taxa. We investigate whether interactions with multiple prey species explain spatially structured variation in the skin toxins of the neotropical poison frog Oophaga pumilio. Specifically, we assess how dissimilarity (i.e., beta diversity) of alkaloid-bearing arthropod prey assemblages (68 ant species) and evolutionary divergence between frog populations (from a neutral genetic marker) contribute to frog poison dissimilarity (toxin profiles composed of 230 different lipophilic alkaloids sampled from 934 frogs at 46 sites). We find that models that incorporate spatial turnover in the composition of ant assemblages explain part of the frog alkaloid variation, and we infer unique alkaloid combinations across the range of O. pumilio. Moreover, we find that alkaloid variation increases weakly with the evolutionary divergence between frog populations. Our results pose two hypotheses: First, the distribution of only a few prey species may explain most of the geographic variation in poison frog alkaloids; second, different codistributed prey species may be redundant alkaloid sources. The analytical framework proposed here can be extended to other multitrophic systems, coevolutionary mosaics, microbial assemblages, and ecosystem services.

PaleoClim, high spatial resolution paleoclimate surfaces for global land areas.

High-resolution, easily accessible paleoclimate data are essential for environmental, evolutionary, and ecological studies. The availability of bioclimatic layers derived from climatic simulations representing conditions of the Late Pleistocene and Holocene has revolutionized the study of species responses to Late Quaternary climate change. Yet, integrative studies of the impacts of climate change in the Early Pleistocene and Pliocene - periods in which recent speciation events are known to concentrate - have been hindered by the limited availability of downloadable, user-friendly climatic descriptors. Here we present PaleoClim, a free database of downscaled paleoclimate outputs at 2.5-minute resolution (~5 km at equator) that includes surface temperature and precipitation estimates from snapshot-style climate model simulations using HadCM3, a version of the UK Met Office Hadley Centre General Circulation Model. As of now, the database contains climatic data for three key time periods spanning from 3.3 to 0.787 million years ago: the Marine Isotope Stage 19 (MIS19) in the Pleistocene (~787 ka), the mid-Pliocene Warm Period (~3.264-3.025 Ma), and MIS M2 in the Late Pliocene (~3.3 Ma).

A mid-Pleistocene rainforest corridor enabled synchronous invasions of the Atlantic Forest by Amazonian anole lizards.

Shifts in the geographic distribution of habitats over time can promote dispersal and vicariance, thereby influencing large-scale biogeographic patterns and ecological processes. An example is that of transient corridors of suitable habitat across disjunct but ecologically similar regions, which have been associated with climate change over time. Such connections likely played a role in the assembly of tropical communities, especially within the highly diverse Amazonian and Atlantic rainforests of South America. Although these forests are presently separated by open and dry ecosystems, paleoclimatic and phylogenetic evidence suggest that they have been transiently connected in the past. However, little is known about the timing, magnitude and the distribution of former forest connections. We employ sequence data at multiple loci from three codistributed arboreal lizards (Anolis punctatus, Anolis ortonii and Polychrus marmoratus) to infer the phylogenetic relationships among Amazonian and Atlantic Forest populations and to test alternative historical demographic scenarios of colonization and vicariance using coalescent simulations and approximate Bayesian computation (ABC). Data from the better-sampled Anolis species support colonization of the Atlantic Forest from eastern Amazonia. Hierarchical ABC indicates that the three species colonized the Atlantic Forest synchronously during the mid-Pleistocene. We find support of population bottlenecks associated with founder events in the two Anolis, but not in P. marmoratus, consistently with their distinct ecological tolerances. Our findings support that climatic fluctuations provided key opportunities for dispersal and forest colonization in eastern South America through the cessation of environmental barriers. Evidence of species-specific histories strengthens assertions that biological attributes play a role in responses to shared environmental change.

Inferring responses to climate dynamics from historical demography in neotropical forest lizards.

We apply a comparative framework to test for concerted demographic changes in response to climate shifts in the neotropical lowland forests, learning from the past to inform projections of the future. Using reduced genomic (SNP) data from three lizard species codistributed in Amazonia and the Atlantic Forest (Anolis punctatus, Anolis ortonii, and Polychrus marmoratus), we first reconstruct former population history and test for assemblage-level responses to cycles of moisture transport recently implicated in changes of forest distribution during the Late Quaternary. We find support for population shifts within the time frame of inferred precipitation fluctuations (the last 250,000 y) but detect idiosyncratic responses across species and uniformity of within-species responses across forest regions. These results are incongruent with expectations of concerted population expansion in response to increased rainfall and fail to detect out-of-phase demographic syndromes (expansions vs. contractions) across forest regions. Using reduced genomic data to infer species-specific demographical parameters, we then model the plausible spatial distribution of genetic diversity in the Atlantic Forest into future climates (2080) under a medium carbon emission trajectory. The models forecast very distinct trajectories for the lizard species, reflecting unique estimated population densities and dispersal abilities. Ecological and demographic constraints seemingly lead to distinct and asynchronous responses to climatic regimes in the tropics, even among similarly distributed taxa. Incorporating such constraints is key to improve modeling of the distribution of biodiversity in the past and future.

Predicting the genetic consequences of future climate change: The power of coupling spatial demography, the coalescent, and historical landscape changes.

PREMISE OF THE STUDY: Climate change is a widely accepted threat to biodiversity. Species distribution models (SDMs) are used to forecast whether and how species distributions may track these changes. Yet, SDMs generally fail to account for genetic and demographic processes, limiting population-level inferences. We still do not understand how predicted environmental shifts will impact the spatial distribution of genetic diversity within taxa. METHODS: We propose a novel method that predicts spatially explicit genetic and demographic landscapes of populations under future climatic conditions. We use carefully parameterized SDMs as estimates of the spatial distribution of suitable habitats and landscape dispersal permeability under present-day, past, and future conditions. We use empirical genetic data and approximate Bayesian computation to estimate unknown demographic parameters. Finally, we employ these parameters to simulate realistic and complex models of responses to future environmental shifts. We contrast parameterized models under current and future landscapes to quantify the expected magnitude of change. KEY RESULTS: We implement this framework on neutral genetic data available from Penstemon deustus. Our results predict that future climate change will result in geographically widespread declines in genetic diversity in this species. The extent of reduction will heavily depend on the continuity of population networks and deme sizes. CONCLUSIONS: To our knowledge, this is the first study to provide spatially explicit predictions of within-species genetic diversity using climatic, demographic, and genetic data. Our approach accounts for climatic, geographic, and biological complexity. This framework is promising for understanding evolutionary consequences of climate change, and guiding conservation planning.

Revisiting the vanishing refuge model of diversification.

Much of the debate around speciation and historical biogeography has focused on the role of stabilizing selection on the physiological (abiotic) niche, emphasizing how isolation and vicariance, when associated with niche conservatism, may drive tropical speciation. Yet, recent re-emphasis on the ecological dimensions of speciation points to a more prominent role of divergent selection in driving genetic, phenotypic, and niche divergence. The vanishing refuge model (VRM), first described by Vanzolini and Williams (1981), describes a process of diversification through climate-driven habitat fragmentation and exposure to new environments, integrating both vicariance and divergent selection. This model suggests that dynamic climates and peripheral isolates can lead to genetic and functional (i.e., ecological and phenotypic) diversity, resulting in sister taxa that occupy contrasting habitats with abutting distributions. Here, we provide predictions for populations undergoing divergence according to the VRM that encompass habitat dynamics, phylogeography, and phenotypic differentiation across populations. Such integrative analyses can, in principle, differentiate the operation of the VRM from other speciation models. We applied these principles to a lizard species, Coleodactylus meridionalis, which was used to illustrate the model in the original paper. We incorporate data on inferred historic habitat dynamics, phylogeography and thermal physiology to test for divergence between coastal and inland populations in the Atlantic Forest of Brazil. Environmental and genetic analyses are concordant with divergence through the VRM, yet physiological data are not. We emphasize the importance of multidisciplinary approaches to test this and alternative speciation models while seeking to explain the extraordinarily high genetic and phenotypic diversity of tropical biomes.

Latitude, elevational climatic zonation and speciation in New World vertebrates.

Many biodiversity hotspots are located in montane regions, especially in the tropics. A possible explanation for this pattern is that the narrow thermal tolerances of tropical species and greater climatic stratification of tropical mountains create more opportunities for climate-associated parapatric or allopatric speciation in the tropics relative to the temperate zone. However, it is unclear whether a general relationship exists among latitude, climatic zonation and the ecology of speciation. Recent taxon-specific studies obtained different results regarding the role of climate in speciation in tropical versus temperate areas. Here, we quantify overlap in the climatic distributions of 93 pairs of sister species of mammals, birds, amphibians and reptiles restricted to either the New World tropics or to the Northern temperate zone. We show that elevational ranges of tropical- and temperate-zone species do not differ from one another, yet the temperature range experienced by species in the temperate zone is greater than for those in the tropics. Moreover, tropical sister species tend to exhibit greater similarity in their climatic distributions than temperate sister species. This pattern suggests that evolutionary conservatism in the thermal niches of tropical taxa, coupled with the greater thermal zonation of tropical mountains, may result in increased opportunities for allopatric isolation, speciation and the accumulation of species in tropical montane regions. Our study exemplifies the power of combining phylogenetic and spatial datasets of global climatic variation to explore evolutionary (rather than purely ecological) explanations for the high biodiversity of tropical montane regions.

Variable responses of skinks to a common history of rainforest fluctuation: concordance between phylogeography and palaeo-distribution models.

There is a growing appreciation of impacts of late-Quaternary climate fluctuations on spatial patterns of species and genetic diversity. A major challenge is to understand how and why species respond individualistically to a common history of climate-induced habitat fluctuation. Here, we combine modelling of palaeo-distributions and mitochondrial-DNA phylogeographies to compare spatial patterns of population persistence and isolation across three species of rainforest skinks (Saproscincus spp.) with varying climatic preferences. Using Akaike Information Criterion model-averaged projections, all three species are predicted to have maintained one or more small populations in the northern Wet Tropics, multiple or larger populations in the central region, and few if any in the south. For the high-elevation species, Saproscincus czechurai, the warm-wet climate of the mid Holocene was most restrictive, whereas for the generalist S. basiliscus and lower-elevation S. tetradactyla, the cool-dry last glacial maximum was most restrictive. As expected, S. czechurai was the most genetically structured species, although relative to modelled distributions, S. basiliscus had surprisingly deep phylogeographical structure among southern rainforest isolates, implying long-term isolation and persistence. For both S. basiliscus and S. tetradactyla, there was high genetic diversity and complex phylogeographical patterns in the central Wet Tropics, reflecting persistence of large, structured populations. A previously identified vicariant barrier separating northern and central regions is supported, and results from these species also emphasize a historical persistence of populations south of another biogeographical break, the Tully Gorge. Overall, the results support the contention that in a topographically heterogeneous landscape, species with broader climatic niches may maintain higher and more structured genetic diversity due to persistence through varying climates.