Christopher J. Schneider

INTEGRATING PHYLOGENETICS AND ENVIRONMENTAL NICHE MODELS TO EXPLORE SPECIATION MECHANISMS IN DENDROBATID FROGS

Abstract We developed an approach that combines distribution data, environmental geographic information system layers, environmental niche models, and phylogenetic information to investigate speciation processes. We used Ecuadorian frogs of the family Dendrobatidae to illustrate our methodology. For dendrobatids there are several cases for which there is significant environmental divergence for allopatric and parapatric lineages. The consistent pattern that many related taxa or nodes exist in distinct environmental space reinforces Lynch and Duellmans hypothesis that differential selection likely played an important role in species differentiation of frogs in the Andes. There is also some evidence that the Río Esmeraldas basin is a geographic barrier to species distributed in low to middle elevations on the western side of the Andes. Another useful aspect of this approach is that it can point to common environmental parameters that correlate with speciation. For dendrobatids, sister clades generally segregate along temperature/elevational and/or seasonality axes. The joint analysis of environmental and geographic data for this group of dendrobatid frogs has identified potentially important speciation mechanisms and specific sister lineages that warrant intensive study to test hypotheses generated in this investigation. Further, the method outlined in this paper will be increasingly useful as knowledge of distribution and phylogeny of tropical species increases.

The genome of the green anole lizard and a comparative analysis with birds and mammals

The evolution of the amniotic egg was one of the great evolutionary innovations in the history of life, freeing vertebrates from an obligatory connection to water and thus permitting the conquest of terrestrial environments. Among amniotes, genome sequences are available for mammals and birds, but not for non-avian reptiles. Here we report the genome sequence of the North American green anole lizard, Anolis carolinensis. We find that A. carolinensis microchromosomes are highly syntenic with chicken microchromosomes, yet do not exhibit the high GC and low repeat content that are characteristic of avian microchromosomes. Also, A. carolinensis mobile elements are very young and diverse—more so than in any other sequenced amniote genome. The GC content of this lizard genome is also unusual in its homogeneity, unlike the regionally variable GC content found in mammals and birds. We describe and assign sequence to the previously unknown A. carolinensis X chromosome. Comparative gene analysis shows that amniote egg proteins have evolved significantly more rapidly than other proteins. An anole phylogeny resolves basal branches to illuminate the history of their repeated adaptive radiations.

Biodiversity hotspots and beyond: the need for preserving environmental transitions

A great deal of effort and many resources are directed at identifying and conserving regions of high species diversity 1xBiodiversity hotspots for conservation priorities. Myers, N. et al. Nature. 2000; 403: 853–858Crossref | PubMed | Scopus (9363)See all References, 2xBiodiversity, hotspots and defiance. Kitching, R. Trends Ecol. Evol. 2000; 15: 484–485Abstract | Full Text | Full Text PDF | Scopus (8)See all References. Although defining ‘biodiversity hotspots’ helps prioritize areas for conservation, overemphasis on such sites ignores the need for preserving adaptive variation across environments. A more comprehensive approach would be to include regions important to the generation and maintenance of biodiversity, regardless of whether they are ‘species rich’. With climate change threatening large-scale shifts in species distributions and the habitats on which they depend, the hotspots of today are unlikely to be the hotspots of tomorrow. Only by maximizing adaptive variation can one hope to preserve the evolutionary response to changing climate and environmental conditions.The ‘hotspot’ approach to species preservation is risky, particularly when applied at a local scale. Preserving populations in only one pure habitat type, such as central tropical rainforests, is analogous to building an investment portfolio made up of a single stock. Diversifying risk by conserving populations from across diverse habitats will ensure that adaptive variation is maximized. Species are assemblages of populations that are often distributed across a landscape of habitat types and those populations have specific adaptations to regional environmental conditions. Populations are being lost at a much higher rate than are species 3xPopulation diversity: its extent and extinction. Hughes, J.B. et al. Science. 1997; 278: 689–692Crossref | PubMed | Scopus (290)See all References3 and, consequently, the loss of populations in unique habitats could result in the loss of novel adaptations that are necessary to meet future environmental challenges 4xConsidering evolutionary processes in conservation biology. Crandall, K.A. et al. Trends Ecol. Evol. 2000; 15: 290–295Abstract | Full Text | Full Text PDF | PubMed | Scopus (990)See all References4. A strategy is urgently needed that preserves the adaptive diversity represented by the range of populations within a species, thus assuring the maximum potential of that species to respond to future environmental conditions.We believe that one strategy for conserving the maximum amount of adaptive variation is to preserve populations that occur along environmental gradients, thus preserving the full range of populations across habitats, as well as the unique traits of those populations. Adaptive diversity within species is often well represented along environmental gradients or ecotones that represent the transition from one habitat type (e.g. tropical rainforest) to another (e.g. grassland or savanna) 5xEndler, J.A. See all References5. Recent research on a wide range of taxa suggests that environmental gradients are important in diversification and speciation 6xSchluter, D. See all References, 7xEcotone: speciation-prone. Schilthuizen, M. Trends Ecol. Evol. 2000; 15: 130–131Abstract | Full Text | Full Text PDF | PubMed | Scopus (44)See all References, 8xNonrandom mating in Drosophila melanogaster laboratory populations derived from closely adjacent ecologically contrasting slopes at ‘Evolution Canyon’. Korol, A. et al. Proc. Natl. Acad. Sci. U. S. A. 2000; 97: 12637–12642Crossref | PubMed | Scopus (79)See all References, 9xRapid evolution of reproductive isolation in the wild: evidence from introduced salmon. Hendry, A.P. et al. Science. 2000; 290: 516–518Crossref | PubMed | Scopus (333)See all References.There is little current emphasis on the conservation of ecological gradients. Recent attempts to prioritize conservation areas ignore these regions entirely 1xBiodiversity hotspots for conservation priorities. Myers, N. et al. Nature. 2000; 403: 853–858Crossref | PubMed | Scopus (9363)See all References, 10xThe Global 200: A representation approach to conserving the Earths most biologically valuable ecoregions. Olson, D.M. and Dinerstein, E. Conserv. Biol. 1998; 12: 502–515CrossrefSee all References. We maintain that a more sound conservation strategy would focus on both hotspots of biodiversity and on associated transitional zones. Given future uncertainty, preserving such areas will maximize the probability of a viable response at the species level to changing climatic conditions. In the absence of extensive data on population variation, we suggest that this diversity is likely to be summarized along environmental gradients. Saving the biota of the Earth will require greater efforts to preserve not only the pattern of biodiversity but also the processes that generate and maintain it. Integrating information on both pattern and process will ensure that the capacity for populations to change with changing environments is preserved.

Acoustic divergence in two cryptic Hipposideros species: a role for social selection?

We present evidence that a relatively widespread and common bat from South East Asia comprises two morphologically cryptic but acoustically divergent species. A population of the bicoloured leaf–nosed bat (Hipposideros bicolor) from Peninsular Malaysia exhibits a bimodal distribution of echolocation call frequencies, with peaks in the frequency of maximum energy at ca. 131 and 142 kHz. The two phonic types are genetically distinct, with a cytochrome b sequence divergence of just under 7%. We consider the mechanisms by which acoustic divergence in these species might arise. Differences in call frequency are not likely to effect resource partitioning by detectable prey size or functional range. However, ecological segregation may be achieved by differences in microhabitat use; the 131 kHz H. bicolor is characterized by significantly longer forearms, lower wing loading, a lower aspect ratio and a more rounded wingtip, features that are associated with greater manoeuvrability in flight that may enable it to forage in more cluttered environments relative to the 142 kHz phonic type. We suggest that acoustic divergence in these species is a consequence of social selection for a clear communication channel, which is mediated by the close link between the acoustic signal and receptor systems imposed by the highly specialized nature of the hipposiderid and rhinolophid echolocation system.

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.

Unraveling the thread of nature’s tapestry: the genetics of diversity and convergence in animal pigmentation

Animals display incredibly diverse color patterns yet little is known about the underlying genetic basis of these phenotypes. However, emerging results are reshaping our view of how the process of phenotypic evolution occurs. Here, we outline recent research from three particularly active areas of investigation: melanin pigmentation in Drosophila, wing patterning in butterflies, and pigment variation in lizards. For each system, we highlight (i) the function and evolution of color variation, (ii) various approaches that have been used to explore the genetic basis of pigment variation, and (iii) conclusions regarding the genetic basis of convergent evolution which have emerged from comparative analyses. Results from these studies indicate that natural variation in pigmentation is a particularly powerful tool to examine the molecular basis of evolution, especially with regard to convergent or parallel evolution. Comparison of these systems also reveals that the molecular basis of convergent evolution is heterogeneous, sometimes involving conserved mechanisms and sometimes not. In the near future, additional work in other emerging systems will substantially expand the scope of available comparisons.

Refugial isolation versus ecological gradients

Hypotheses for divergence and speciation in rainforests generally fall into two categories: those emphasizing the role of geographic isolation and those emphasizing the role of divergent selection along gradients. While a majority of studies have attempted to infer mechanisms based on the pattern of species richness and congruence of geographic boundaries, relatively few have tried to simultaneously test alternative hypotheses for diversification. Here we discuss four examples, taken from our work on diversification of tropical rainforest vertebrates, in which we examine patterns of genetic and morphological variation within and between biogeographic regions to address two alternative hypotheses. By estimating morphological divergence between geographically contiguous and isolated populations under similar and different ecological conditions, we attempt to evaluate the relative roles of geographic isolation and natural selection in population divergence. Results suggest that natural selection, even in the presence of appreciable gene flow, can result in morphological divergence that is greater than that found between populations isolated for millions of years and, in some cases, even greater than that found between congeneric, but distinct, species. The relatively small phenotypic divergence that occurs among long-term geographic isolates in similar habitats suggests that morphological divergence via drift may be negligible and/or that selection is acting to produce similar phenotypes in populations occupying similar habitats. Our results demonstrate that significant phenotypic divergence: (1) is not necessarily coupled with divergence in neutral molecular markers; and (2) can occur without geographic isolation in the presence of gene flow.

Mapping evolutionary process: a multi‐taxa approach to conservation prioritization

Human‐induced land use changes are causing extensive habitat fragmentation. As a result, many species are not able to shift their ranges in response to climate change and will likely need to adapt in situ to changing climate conditions. Consequently, a prudent strategy to maintain the ability of populations to adapt is to focus conservation efforts on areas where levels of intraspecific variation are high. By doing so, the potential for an evolutionary response to environmental change is maximized. Here, we use modeling approaches in conjunction with environmental variables to model species distributions and patterns of genetic and morphological variation in seven Ecuadorian amphibian, bird, and mammal species. We then used reserve selection software to prioritize areas for conservation based on intraspecific variation or species‐level diversity. Reserves selected using species richness and complementarity showed little overlap with those based on genetic and morphological variation. Priority areas for intraspecific variation were mainly located along the slopes of the Andes and were largely concordant among species, but were not well represented in existing reserves. Our results imply that in order to maximize representation of intraspecific variation in reserves, genetic and morphological variation should be included in conservation prioritization.

Comparative population structure of Cynopterus fruit bats in peninsular Malaysia and southern Thailand

The extent to which response to environmental change is mediated by species‐specific ecology is an important aspect of the population histories of tropical taxa. During the Pleistocene glacial cycles and associated sea level fluctuations, the Sunda region in Southeast Asia experienced concurrent changes in landmass area and the ratio of forest to open habitat, providing an ideal setting to test the expectation that habitat associations played an important role in determining species’ response to the opportunity for geographic expansion. We used mitochondrial control region sequences and six microsatellite loci to compare the phylogeographic structure and demographic histories of four broadly sympatric species of Old World fruit bats in the genus, Cynopterus. Two forest‐associated species and two open‐habitat generalists were sampled along a latitudinal transect in Singapore, peninsular Malaysia, and southern Thailand. Contrary to expectations based on habitat associations, the geographic scale of population structure was not concordant across ecologically similar species. We found evidence for long and relatively stable demographic history in one forest and one open‐habitat species, and inferred non‐coincident demographic expansions in the second forest and open‐habitat species. Thus, while these results indicate that Pleistocene climate change did not have a single effect on population structure across species, a correlation between habitat association and response to environmental change was supported in only two of four species. We conclude that interactions between multiple factors, including historical and contemporary environmental change, species‐specific ecology and interspecific interactions, have shaped the recent evolutionary histories of Cynopterus fruit bats in Southeast Asia.

Modeling environmentally associated morphological and genetic variation in a rainforest bird, and its application to conservation prioritization.

To better understand how environment shapes phenotypic and genetic variation, we explore the relationship between environmental variables across Ecuador and genetic and morphological variation in the wedge‐billed woodcreeper (Glyphorynchus spirurus), a common Neotropical rainforest bird species. Generalized dissimilarity models show that variation in amplified fragment length polymorphism markers was strongly associated with environmental variables on both sides of the Andes, but could also partially be explained by geographic distance on the western side of the Andes. Tarsus, wing, tail, and bill lengths and bill depth were well explained by environmental variables on the western side of the Andes, whereas only tarsus length was well explained on the eastern side. Regions that comprise the highest rates of genetic and phenotypic change occur along steep elevation gradients in the Andes. Such environmental gradients are likely to be particularly important for maximizing adaptive diversity to minimize the impacts of climate change. Using a framework for conservation prioritization based on preserving ecological and evolutionary processes, we found little overlap between currently protected areas in Ecuador and regions we predicted to be important in maximizing adaptive variation.