Rugged relief and climate promote isolation and divergence between two neotropical cold-associated birds.

The role of historical factors in establishing patterns of diversity in tropical mountains is of interest to understand the buildup of megadiverse biotas. In these regions, the historical processes of range fragmentation and contraction followed by dispersal are thought to be mediated by the interplay between rugged relief (complex topography) and climate fluctuations and likely explain most of the dynamics of diversification in plants and animals. Although empirical studies addressing the interaction between climate and topography have provided invaluable insights into population divergence and speciation patterns in tropical montane organisms, a more detailed and robust test of such processes in an explicit spatio-temporal framework is still lacking. Consequently, our ability to gain insights into historical range shifts over time and the genomic footprint left by them is limited. Here, we used niche modeling and subgenomic population-level datasets to explore the evolution of two species of warbling finches (genus Microspingus) disjunctly distributed across the Montane Atlantic Forest, a Neotropical region with complex geological and environmental histories. Population structure inferences suggest a scenario of three genetically differentiated populations, which are congruent with both geography and phenotypic variation. Demographic simulations support asynchronous isolation of these populations as recently as ∼40,000 years ago, relatively stable population sizes over recent time, and past gene flow subsequent to divergence. Throughout the last 800,000 years, niche models predicted extensive expansion into lowland areas with increasing overlap of species distributions during glacial periods, with prominent retractions and isolation into higher altitudes during interglacials, which are in line with signs of introgression of currently isolated populations. These results support a dual role of cyclical climatic changes: population divergence and persistence in mountain tops during warm periods followed by periods of expansion and admixture in lower elevations during cold periods. Our results underscore the role of the interplay between landscape and climate as an important mechanism in the evolution of the Neotropical montane biota.

The relative contribution of natural landscapes and human-mediated factors on the connectivity of a noxious invasive weed.

Examining how the landscape may influence gene flow is at the forefront of understanding population differentiation and adaptation. Such understanding is crucial in light of ongoing environmental changes and the elevated risk of ecosystems alteration. In particular, knowledge of how humans may influence population structure is imperative to allow for informed decisions in management and conservation as well as to gain a better understanding of anthropogenic impacts on the interplay between gene flow, genetic drift, and selection. Here, we use genome-wide molecular markers to characterize the population genetic structure and connectivity of Ipomoea purpurea (Convolvulaceae), a noxious invasive weed. We, likewise, assess the interaction between natural and human-driven influences on genetic differentiation among populations. Our analyses find that human population density is an important predictor of pairwise population differentiation, suggesting that the agricultural and/or horticultural trade may be involved in maintaining some level of connectivity across distant agricultural fields. Climatic variation appears as an additional predictor of genetic connectivity in this species. We discuss the implications of these results and highlight future research needed to disentangle the mechanistic processes underlying population connectivity of weeds.

Natural and Anthropogenic Influences on the Mating System of the Common Morning Glory.

Evolutionary biologists remain puzzled by the often dramatic variation of mating strategies within single species. Of particular interest is the extent to which environmental conditions shape patterns of variation of mating system components within mixed mating species, and how widespread anthropogenic manipulations may influence these associations. Here, we address this question in the common morning glory (Ipomoea purpurea) by combining a dataset of floral traits, estimates of the mating system, and relevant environmental factors compiled for 22 populations of this species distributed along a wide range of environments from the Southeastern and Midwestern United States. We identify a disparate set of environmental factors to influence population-level variation in selfing, inbreeding, and flower morphology. Although floral traits are primarily associated with climatic variation, the outcrossing rate and inbreeding coefficient are primarily influenced by the level of herbicide resistance. Furthermore, we find that populations with higher levels of herbicide resistance exhibit a stronger correlation between mating system-floral traits and mating system estimates (outcrossing rate and inbreeding coefficient). Altogether, these results demonstrate the dominant role that herbicide application plays in the determination of I. purpurea's mating system, and more generally uncover the complex and unforeseen evolutionary consequences of anthropogenic manipulations in natural systems.

Comment on Rieux and Balloux: calibration from tip-dating can compromise topological accuracy and evolutionary inference.

We contribute to the recent review of Rieux & Balloux, 2016, Mol. Ecol., 25, 1911 on inferences from tip-dated phylogenies by developing their discussion on the influence of population size (Ne ) under panmixia for the estimation of substitution rate (µ). We highlight how phylogenetic trees inferred with tip-dated sequences under large panmictic Ne tend to erroneously enforce an age-based coalescent pattern on the posterior distribution of trees, which in turn results in systematically inflated estimates of µ. We discuss the consequences of this and suggest how to accommodate the issue in the short term and long term.

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.

Urbanization shapes the demographic history of a native rodent (the white-footed mouse, Peromyscus leucopus) in New York City.

How urbanization shapes population genomic diversity and evolution of urban wildlife is largely unexplored. We investigated the impact of urbanization on white-footed mice,Peromyscus leucopus,in the New York City (NYC) metropolitan area using coalescent-based simulations to infer demographic history from the site-frequency spectrum. We assigned individuals to evolutionary clusters and then inferred recent divergence times, population size changes and migration using genome-wide single nucleotide polymorphisms genotyped in 23 populations sampled along an urban-to-rural gradient. Both prehistoric climatic events and recent urbanization impacted these populations. Our modelling indicates that post-glacial sea-level rise led to isolation of mainland and Long Island populations. These models also indicate that several urban parks represent recently isolated P. leucopus populations, and the estimated divergence times for these populations are consistent with the history of urbanization in NYC.

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.

Model misspecification confounds the estimation of rates and exaggerates their time dependency.

While welcoming the comment of Ho et al. (2015), we find little that undermines the strength of our criticism, and it would appear they have misunderstood our central argument. Here we respond with the purpose of reiterating that we are (i) generally critical of much of the evidence presented in support of the time-dependent molecular rate (TDMR) hypothesis and (ii) specifically critical of estimates of µ derived from tip-dated sequences that exaggerate the importance of purifying selection as an explanation for TDMR over extended timescales. In response to assertions put forward by Ho et al. (2015), we use panmictic coalescent simulations of temporal data to explore a fundamental assumption for tip-dated tree shape and associated mutation rate estimates, and the appropriateness and utility of the date randomization test. The results reveal problems for the joint estimation of tree topology, effective population size and µ with tip-dated sequences using BEAST. Given the simulations, BEAST consistently obtains incorrect topological tree structures that are consistent with the substantial overestimation of µ and underestimation of effective population size. Data generated from lower effective population sizes were less likely to fail the date randomization test yet still resulted in substantially upwardly biased estimates of rates, bringing previous estimates of µ from temporally sampled DNA sequences into question. We find that our general criticisms of both the hypothesis of time-dependent molecular evolution and Bayesian methods to estimate µ from temporally sampled DNA sequences are further reinforced.

Ecological niche models in phylogeographic studies: applications, advances and precautions.

The increased availability of spatial data and methodological developments in species distribution modelling has lead to concurrent advances in phylogeography, broadening the scope of questions studied, as well as providing unprecedented insights. Given the species-specific nature of the information provided by ecological niche models (ENMs), whether it is on the environmental tolerances of species or their estimated distribution, today or in the past, it is perhaps not surprising that ENMs have rapidly become a common tool in phylogeographic analysis. Such information is essential to phylogeographic tests that provide important biological insights. Here, we provide an overview of the different applications of ENMs in phylogeographic studies, detailing specific studies and highlighting general limitations and challenges with each application. Given that the full potential of integrating ENMs into phylogeographic cannot be realized unless the ENMs themselves are carefully applied, we provide a summary of best practices with using ENMs. Lastly, we describe some recent advances in how quantitative information from ENMs can be integrated into genetic analyses, illustrating their potential use (and key concerns with such implementations), as well as promising areas for future development.

Localized versus generalist phenotypes in a broadly distributed tropical mammal: how is intraspecific variation distributed across disparate environments?

BACKGROUND: The extent of phenotypic differentiation in response to local environmental conditions is a key component of species adaptation and persistence. Understanding the structuring of phenotypic diversity in response to local environmental pressures can provide important insights into species evolutionary dynamics and responses to environmental change. This work examines the influence of steep environmental gradients on intraspecific phenotypic variation and tests two hypotheses about how the tropical soft grass mouse, Akodon mollis (Cricetidae, Rodentia), contends with the disparate environmental conditions encompassed by its broad distribution. Specifically, we test if the species expresses a geographically unstructured, or generalist, phenotype throughout its range or if it shows geographically localized morphological differentiation across disparate environments. RESULTS: Using geometric morphometric and ecomorphological analyses of skull shape variation we found that despite distinct environmental conditions, geographically structured morphological variation is limited, with the notable exception of a distinct morphological disjunction at the high-elevation forest-grassland transition in the southern portion of A. mollis distribution. Based on genetic analyses, geographic isolation alone does not explain this localized phenotype, given that similar levels of genetic differentiation were also observed among individuals inhabiting other ecosystems that are nonetheless not distinct morphologically. CONCLUSIONS: Instead of phenotypic specialization across environments in these tropical mountains, there was limited differentiation of skull shape and size across the broad range of A. mollis, with the exception of individuals from the puna, the highest-elevation ecosystem. The high morphological variance among individuals, together with a weak association with local environmental conditions, not only highlights the flexibility of A. mollis' skull, but also highlights the need for further study to understand what maintains the observed morphological patterns. The work also indicates that mechanisms other than processes linked to local ecological specialization as a driver of diversification may contribute to the high diversity of this tropical region.

Exploring the population genetic consequences of the colonization process with spatio-temporally explicit models: insights from coupled ecological, demographic and genetic models in montane grasshoppers.

Understanding the genetic consequences of shifting species distributions is critical for evaluating the impact of climate-induced distributional changes. However, the demographic expansion associated with the colonization process typically takes place across a heterogeneous environment, with population sizes and migration rates varying across the landscape. Here we describe an approach for coupling ecological-niche models (ENMs) with demographic and genetic models to explore the genetic consequences of distributional shifts across a heterogeneous landscape. Analyses of a flightless grasshopper from the sky islands of the Rocky Mountains of North America are used to show how biologically informed predictions can be generated about the genetic consequences of a colonization process across a spatially and temporally heterogeneous landscape (i.e. the suitability of habitats for the montane species differs across the landscape and is itself not static, with the displacement of contemporary populations into glacial refugia). By using (i) ENMs for current climatic conditions and the last glacial maximum to (ii) parameterize a demographic model of the colonization process, which then (iii) informs coalescent simulations, a set of models can be generated that capture different processes associated with distributional shifts. We discuss how the proposed approach for model generation can be integrated into a statistical framework for estimating key demographic parameters and testing hypotheses about the conditions for which distributional shifts may (or may not) enhance species divergence, including the importance of habitat stability, past gene-flow among currently isolated populations, and maintenance of refugial populations in multiple geographic regions.