Genetic diversity and ecological niche modelling of the restricted Recordia reitzii (Verbenaceae) from southern Brazilian Atlantic forest

Genetic diversity analyses, coupled with ecological niche modelling (ENM) of species with a restricted distribution, may provide valuable information for understanding diversification patterns in endangered areas. We analyzed the genetic diversity of Recordia reitzii, a tree restricted to the threatened and highly fragmented Brazilian Atlantic forest, using three intergenic cpDNA spacers and ten microsatellite (SSR) loci. To assess the historical processes that may have influenced the distribution of extant R. reitzii populations, the current potential distributions of R. reitzii and Recordia boliviana, a closely related species, were modelled and projected onto the Last Glacial Maximum (LGM) and Last Interglacial (LIG) periods. Niche divergence was quantified between these two. The cpDNA and SSR data showed a north–south pattern of the diversity distribution and structured populations, suggesting that gene flow is probably limited. According to our data, R. reitzii exhibits low genetic diversity, which may be a result of a founder or distribution‐reduction effect, narrow distribution or small population size. The ecological niche models showed a wider palaeodistribution during the LIG and a retraction during the LGM for both species. Tests of niche divergence and conservatism indicated that bioclimatic factors might have influenced the diversification of these Recordia species. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 176 , 332–348.     

Testing ecological explanations for biogeographic boundaries

Barriers to dispersal and resulting biogeographic boundaries are responsible for much of life's diversity. Distinguishing the contribution of ecological, historical, and stochastic processes to the origin and maintenance of biogeographic boundaries, however, is a longstanding challenge. Taking advantage of newly available data and methods--including environmental niche models and associated comparative metrics--we develop a framework to test two possible ecological explanations for biogeographic boundaries: (1) sharp environmental gradients and (2) ribbons of unsuitable habitat dividing two highly suitable regions. We test each of these hypotheses against the null expectation that environmental variation across a given boundary is no greater than expected by chance. We apply this framework to a pair of Hispaniolan Anolis lizards (A. chlorocyanus and A. coelestinus) distributed on the either side of this island's most important biogeographic boundary. Integrating our results with historical biogeographic analysis, we find that a ribbon of particularly unsuitable habitat is acting to maintain a boundary between species that initially diverged on distinct paleo-islands, which merged to form present-day Hispaniola in the Miocene.     

Testing the role of climate in speciation: New methods and applications to squamate reptiles (lizards and snakes)

Climate may play important roles in speciation, such as causing the range fragmentation that underlies allopatric speciation (through niche conservatism) or driving divergence of parapatric populations along climatic gradients (through niche divergence). Here, we developed new methods to test the frequency of climate niche conservatism and divergence in speciation, and applied it to species pairs of squamate reptiles (lizards and snakes). We used a large‐scale phylogeny to identify 242 sister species pairs for analysis. From these, we selected all terrestrial allopatric pairs with sufficient occurrence records (n = 49 pairs) and inferred whether each originated via climatic niche conservatism or climatic niche divergence. Among the 242 pairs, allopatric pairs were most common (41.3%), rather than parapatric (19.4%), partially sympatric (17.7%), or fully sympatric species pairs (21.5%). Among the 49 selected allopatric pairs, most appeared to have originated via climatic niche divergence (61–76%, depending on the details of the methods). Surprisingly, we found greater climatic niche divergence between allopatric sister species than between parapatric pairs, even after correcting for geographic distance. We also found that niche divergence did not increase with time, further implicating niche divergence in driving lineage splitting. Overall, our results suggest that climatic niche divergence may often play an important role in allopatric speciation, and the methodology developed here can be used to address the generality of these findings in other organisms.     

Niche shift can impair the ability to predict invasion risk in the marine realm: an illustration using Mediterranean fish invaders

Climatic niche conservatism, the tendency of species‐climate associations to remain unchanged across space and time, is pivotal for forecasting the spread of invasive species and biodiversity changes. Indeed, it represents one of the key assumptions underlying species distribution models (SDMs), the main tool currently available for predicting range shifts of species. However, to date, no comprehensive assessment of niche conservatism is available for the marine realm. We use the invasion by Indo‐Pacific tropical fishes into the Mediterranean Sea, the world's most invaded marine basin, to examine the conservatism of the climatic niche. We show that tropical invaders may spread far beyond their native niches and that SDMs do not predict their new distributions better than null models. Our results suggest that SDMs may underestimate the potential spread of invasive species and call for prudence in employing these models in order to forecast species invasion and their response to environmental change.     

Lineage diversification in a widespread species: roles for niche divergence and conservatism in the common kingsnake, Lampropeltis getula

Niche conservatism and niche divergence are both important ecological mechanisms associated with promoting allopatric speciation across geographical barriers. However, the potential for variable responses in widely distributed organisms has not been fully investigated. For allopatric sister lineages, three patterns for the interaction of ecological niche preference and geographical barriers are possible: (i) niche conservatism at a physical barrier; (ii) niche divergence at a physical barrier; and (iii) niche divergence in the absence of a physical barrier. We test for the presence of these patterns in a transcontinentally distributed snake species, the common kingsnake ( Lampropeltis getula ), to determine the relative frequency of niche conservatism or divergence in a single species complex inhabiting multiple distinct ecoregions. We infer the phylogeographic structure of the kingsnake using a range-wide data set sampled for the mitochondrial gene cytochrome b . We use coalescent simulation methods to test for the presence of structured lineage formation vs. fragmentation of a widespread ancestor. Finally, we use statistical techniques for creating and evaluating ecological niche models to test for conservatism of ecological niche preferences. Significant geographical structure is present in the kingsnake, for which coalescent tests indicate structured population division. Surprisingly, we find evidence for all three patterns of conservatism and divergence. This suggests that ecological niche preferences may be labile on recent phylogenetic timescales, and that lineage formation in widespread species can result from an interaction between inertial tendencies of niche conservatism and natural selection on populations in ecologically divergent habitats.     

Genetic admixture in multidimensional environmental space: asymmetrical niche similarity promotes gene flow in armadillos (Dasypus novemcinctus)

We unite genetic data with a robust test of niche divergence to test the hypothesis that patterns of gene flow between two lineages of the nine-banded armadillo are influenced by their climatic niches. We collected Geographical Information System (GIS) data on climate using locality information from 111 individuals from two lineages that had associated genetic material. We tested whether niches of these lineages were more conserved or divergent than the background environments of their geographic ranges and found evidence for niche conservatism on two axes and no evidence for divergence on any axis. To address the role of niche similarity in gene flow, we genotyped the 111 individuals at five microsatellite loci and tested whether admixed individuals tended to be located in parts of multidimensional environmental space (E-space) shared between the two lineages. We observed an asymmetrical pattern of overlap, in which the West lineage's E-space was almost completely included inside East lineage's E-space. Genetic admixture levels were significantly higher in the West lineage and, for both lineages, in shared portions of E-space. This suggests that niche similarity can facilitate gene flow among disjunct groups with moderate-to-good dispersal capabilities, contrasting with the prevailing view of niche conservatism as a diversifying force.     

HOW IS THE RATE OF CLIMATIC‐NICHE EVOLUTION RELATED TO CLIMATIC‐NICHE BREADTH?

The rate of climatic‐niche evolution is important to many research areas in ecology, evolution, and conservation biology, including responses of species to global climate change, spread of invasive species, speciation, biogeography, and patterns of species richness. Previous studies have implied that clades with higher rates of climatic‐niche evolution among species should have species with narrower niche breadths, but there is also evidence suggesting the opposite pattern. However, the relationships between rate and breadth have not been explicitly analyzed. Here, we examine the relationships between the rate of climatic‐niche evolution and climatic‐niche breadth using phylogenetic and climatic data for 250 species in the salamander family Plethodontidae, a group showing considerable variation in both rates of climatic‐niche evolution and climatic‐niche breadths. Contrary to some expectations, we find no general relationship between climatic‐niche breadth and the rate of climatic‐niche evolution. Climatic‐niche breadths for some ecologically important climatic variables considered separately (temperature seasonality and annual precipitation) do show significant relationships with the rate of climatic‐niche evolution, but rates are faster in clades in which species have broader (not narrower) niche breadths. In summary, our results show that narrower niche breadths are not necessarily associated with faster rates of niche evolution.     

On the evolutionary stability of sink populations

The evolution of adaptive behaviours can influence population dynamics. Conversely, population dynamics can affect both the rate and direction of adaptive evolution. This paper examines reasons why sink populations – populations maintained by immigration, preventing local extinction – might persist in the habitat repertoire of a species over evolutionary time-scales. Two such reasons correspond to standard explanations for deviations from an ideal free habitat distribution: organisms may not be free to settle in whichever habitat has the highest potential fitness, and may be constrained by costs, perceptual limitations, or mode of dispersal in the acuity of their habitat selectivity. Here, I argue that a third general reason for persistent sink populations is provided by unstable population dynamics in source habitats. I present a simple model illustrating how use of a sink habitat may be selectively advantageous, when a source population has unstable dynamics (which necessarily reflects temporal variation in local fitnesses). Species with unstable local dynamics in high-quality habitats should be selected to utilize a broader range of habitats than species with stable local dynamics, and in particular in some circumstances should utilize sink habitats. This observation has implications for the direction of niche evolution, and the likelihood of niche conservatism.     

DOES NICHE DIVERGENCE ACCOMPANY ALLOPATRIC DIVERGENCE IN APHELOCOMA JAYS AS PREDICTED UNDER ECOLOGICAL SPECIATION?: INSIGHTS FROM TESTS WITH NICHE MODELS

The role of ecology in the origin of species has been the subject of long‐standing interest to evolutionary biologists. New sources of spatially explicit ecological data allow for large‐scale tests of whether speciation is associated with niche divergence or whether closely related species tend to be similar ecologically (niche conservatism). Because of the confounding effects of spatial autocorrelation of environmental variables, we generate null expectations for niche divergence for both an ecological‐niche modeling and a multivariate approach to address the question: do allopatrically distributed taxa occupy similar niches? In a classic system for the study of niche evolution—the Aphelocoma jays—we show that there is little evidence for niche divergence among Mexican Jay (A. ultramarina) lineages in the process of speciation, contrary to previous results. In contrast, Aphelocoma species that exist in partial sympatry in some regions show evidence for niche divergence. Our approach is widely applicable to the many cases of allopatric lineages in the beginning stages of speciation. These results do not support an ecological speciation model for Mexican Jay lineages because, in most cases, the allopatric environments they occupy are not significantly more divergent than expected under a null model.     

The phylogenetic signal of diversification rates

Hypotheses to explain the causes of diversity gradients have increasingly focused on the factors that actually change species numbers, namely speciation, extinction and dispersal. A common assumption of many of these hypotheses is that there should be phylogenetic signal in diversification rates, yet this assumption has rarely been tested explicitly. In this study, we compile a large data set including 328,219 species of plants, mammals, amphibians and squamates to assess the level of phylogenetic signal in their diversification rates. Significant phylogenetic signal was detected in all data sets, except for squamates, suggesting not only that closely related clades indeed might share similar diversification rates, but also that the level of phylogenetic signal might vary considerably between them. Moreover, there were intriguing differences among taxa in the rate of decay in phylogenetic autocorrelation over time, underscoring the existence of taxon-specific patterns of phylogenetic autocorrelation. These results have important implications for the development of more realistic models of species diversification.     

Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species

Ecologists are increasingly adopting an evolutionary perspective, and in recent years, the idea that closely related species are ecologically similar has become widespread. In this regard, phylogenetic signal must be distinguished from phylogenetic niche conservatism. Phylogenetic niche conservatism results when closely related species are more ecologically similar that would be expected based on their phylogenetic relationships; its occurrence suggests that some process is constraining divergence among closely related species. In contrast, phylogenetic signal refers to the situation in which ecological similarity between species is related to phylogenetic relatedness; this is the expected outcome of Brownian motion divergence and thus is necessary, but not sufficient, evidence for the existence of phylogenetic niche conservatism. Although many workers consider phylogenetic niche conservatism to be common, a review of case studies indicates that ecological and phylogenetic similarities often are not related. Consequently, ecologists should not assume that phylogenetic niche conservatism exists, but rather should empirically examine the extent to which it occurs.     

The shaping of genetic variation in edge‐of‐range populations under past and future climate change

With rates of climate change exceeding the rate at which many species are able to shift their range or adapt, it is important to understand how future changes are likely to affect biodiversity at all levels of organisation. Understanding past responses and extent of niche conservatism in climatic tolerance can help predict future consequences. We use an integrated approach to determine the genetic consequences of past and future climate changes on a bat species, Plecotus austriacus. Glacial refugia predicted by palaeo‐modelling match those identified from analyses of extant genetic diversity and model‐based inference of demographic history. Former refugial populations currently contain disproportionately high genetic diversity, but niche conservatism, shifts in suitable areas and barriers to migration mean that these hotspots of genetic diversity are under threat from future climate change. Evidence of population decline despite recent northward migration highlights the need to conserve leading‐edge populations for spearheading future range shifts.     

Assessing concurrent patterns of environmental niche and morphological evolution among species of horned lizards (Phrynosoma)

The prediction that variation in species morphology is related to environmental features has long been of interest to ecologists and evolutionary biologists. Many studies have demonstrated strong associations between morphological traits and local habitat characteristics, but few have considered the extent to which morphological traits may be associated with environmental features across broad geographic areas. Here, we use morphological, environmental and phylogenetic data compiled from Phrynosoma species to examine morphological and climatic variation across the geographic ranges of these species in an evolutionary context. We find significant phylogenetic signal in species’ environmental niches, but not in morphological traits. Furthermore, we demonstrate a significant correlation between species’ environmental niches and morphological traits when phylogenetic history is accounted for in the analysis. Our results suggest the importance of climatic variables in influencing morphological variation among species, and have implications for understanding how species distributions are constrained by environmental variation.     

Complex patterns of environmental niche evolution in Iberian columbines (genus Aquilegia,Ranunculaceae)

Aims This study explores the patterns of niche differentiation in a group of seven closely related columbines (genus Aquilegia, Ranunculaceae) from the Iberian Peninsula. Populations of these columbines are subject to complex patterns of divergent selection across environments, which partly explain the taxonomic structure of the group. This suggests the hypothesis that niche divergence must have occurred along the process of diversification of the group.Methods We used MaxEnt to build environmental niche models of seven subspecies belonging to the three species of Aquilegia present in the Iberian Peninsula. From these models, we compared the environmental niches through two different approaches: ENMtools and multivariate methods.Important findings MaxEnt distributions conformed closely to the actual distribution of the study taxa. ENMtools methods failed to uncover any clear patterns of niche differentiation or conservatism in Iberian columbines. Multivariate analyses indicate the existence of differentiation along altitudinal gradients and along a gradient of climatic conditions determined by the summer precipitation and temperatures. However, climatic conditions related to winter temperature and precipitation, as well as soil properties, were equally likely to show conservatism or divergence. The complex patterns of niche evolution we found suggest that Iberian Columbines have not been significantly constrained by forces of niche conservatism, so they could respond adaptively to the fast and profound climate changes in the Iberian Peninsula through the glacial cycles of the Pleistocene.     

LATITUDINAL VARIATION IN SPECIATION MECHANISMS IN FROGS

Speciation often has a strong geographical and environmental component, but the ecological factors that potentially underlie allopatric and parapatric speciation remain understudied. Two ecological mechanisms by which speciation may occur on geographic scales are allopatric speciation through niche conservatism and parapatric or allopatric speciation through niche divergence. A previous study on salamanders found a strong latitudinal pattern in the prevalence of these mechanisms, with niche conservatism dominating in temperate regions and niche divergence dominating in the tropics, and related this pattern to Janzen's hypothesis of greater climatic zonation between different elevations in the tropics. Here, we test for latitudinal patterns in speciation in a related but more diverse group of amphibians, the anurans. Using data from up to 79 sister-species pairs, we test for latitudinal variation in elevational and climatic overlap between sister species, and evaluate the frequency of speciation via niche conservatism versus niche divergence in relation to latitude. In contrast to salamanders, we find no tendency for greater niche divergence in the tropics or for greater niche conservatism in temperate regions. Although our results support the idea of greater climatic zonation in tropical regions, they show that this climatic pattern does not lead to straightforward relationships between speciation, latitude, and niche evolution.