Evolution of climatic niche specialization: a phylogenetic analysis in amphibians

Maria Fernanda Bonetti 1 2 3 John J. Wiens 0 1 3 0 Department of Ecology and Evolutionary Biology, University of Arizona , Tucson, AZ 85721 , USA 1 One contribution to a Special feature 'Evolution of specialization: insights from phylogenetic analysis' 2 Programa de Po s Graduac a o em Ecologia e Conserva ca o, Setor de Ciencias Biolo gicas, Universidade Federal do Parana , Caixa Postal 19031, Curitiba, Parana 81.531-990 , Brazil 3 Subject Areas: evolution , ecology The evolution of climatic niche specialization has important implications for many topics in ecology, evolution and conservation. The climatic niche reflects the set of temperature and precipitation conditions where a species can occur. Thus, specialization to a limited set of climatic conditions can be important for understanding patterns of biogeography, species richness, community structure, allopatric speciation, spread of invasive species and responses to climate change. Nevertheless, the factors that determine climatic niche width (level of specialization) remain poorly explored. Here, we test whether species that occur in more extreme climates are more highly specialized for those conditions, and whether there are trade-offs between niche widths on different climatic niche axes (e.g. do species that tolerate a broad range of temperatures tolerate only a limited range of precipitation regimes?). We test these hypotheses in amphibians, using phylogenetic comparative methods and global-scale datasets, including 2712 species with both climatic and phylogenetic data. Our results do not support either hypothesis. Rather than finding narrower niches in more extreme environments, niches tend to be narrower on one end of a climatic gradient but wider on the other. We also find that temperature and precipitation niche breadths are positively related, rather than showing trade-offs. Finally, our results suggest that most amphibian species occur in relatively warm and dry environments and have relatively narrow climatic niche widths on both of these axes. Thus, they may be especially imperilled by anthropogenic climate change. 1. Introduction Climatic niche specialization is a very specific topic, but one that has surprisingly far-reaching implications. Every terrestrial species has a climatic niche, a set of temperature and precipitation conditions where it occurs [1 3]. The climatic niche is critically important because it may determine where that species occurs (either alone or in combination with other abiotic and biotic factors) and how it will respond to changes in climate over time. But these patterns of geographical distribution and response to climate change depend not only on the climatic niche but also on specialization in that niche (i.e. climatic niche width). If species were not specialized for a limited set of climatic conditions, every species could potentially occur almost anywhere (at least within a continent or island) and anthropogenic climate change would not be problematic for species persistence. But most species do appear to be specialized for a limited set of climatic conditions. For example, few species occur continuously from the poles to the Equator, or from sea level to above treeline within a region, regardless of the specific mechanisms that determine their geographical ranges. Given this, climatic niche specialization appears to have important implications for numerous topics in biogeography, ecology, evolution and conservation. There is now evidence that climatic niche specialization, coupled with climatic niche conservatism (climatic niches remaining similar over time within and among species; reviewed in [4]), can play a role in determining large-scale patterns of biogeography [5,6], patterns of species richness along gradients in latitude [7 10], elevation [11,12] and aridity [13], geographical patterns of community structure [14], allopatric speciation [15 18], patterns of geographical spread in invasive species [19 21] and may determine the responses of species to anthropogenic climate change [22 24]. Of course, climatic specialization is also important when there is climatic divergence, and the combination of climatic niche specialization and divergence may drive other patterns, such as parapatric speciation along environmental gradients and clade diversification [18,25,26]. For example, there would be no ecological speciation along environmental gradients if species were able to occur everywhere along the gradient and were not specialized for a more limited set of conditions. What determines how specialized the climatic niche is in a given species? This question has remained relatively unexplored, especially in comparison to the burgeoning literature that addresses the consequences of specialization, conservatism and divergence in the climatic niche (see references above). Previous studies suggest that several different factors may influence the width of the climatic niche, but some of the most important factors are closely intertwined: these are seasonality, latitude and the specific aspect of the niche that is being considered (i.e. temperature, precipitation). In general, temperature seasonality increases with latitude, but precipitation seasonality decreases with latitude [27,28]. Analyses in three species-rich clades of vertebrates (hylid frogs, plethodontid salamanders and phrynosomatid lizards) suggest that this within-locality seasonality is the major driver of specieslevel niche width for both temperature and precipitation, rather than variation in climatic conditions across the species range [29]. Nevertheless, climatic variation between localities does have a significant (albeit smaller) impact on climatic niche width of species, potentially reflecting the role of local adaptation on the species niche width [29]. A question that is especially poorly explored is whether species that occur in more extreme climatic conditions on a given niche axis (i.e. have extreme niche positions) are more highly specialized for those conditions (figure 1a). For example, does adapting to more extreme or stressful conditions require a trade-off that limits the ability of those species to occur across a broad range of conditions? Or are species that can tolerate more extreme conditions able to do so simply because they can tolerate a broader range of conditions than other species (figure 1b)? Or is there no relationship between the niche width of species and their position on an environmental gradient (figure 1c)? Or does it depend on which end of the gradient is being considered? For example, are species that occur under colder temperatures able to tolerate a broad range of conditions while species that occur in warmer conditions have only a limited range of tolerances (figure 1d )? To our knowledge, only one previous study has addressed the relationship between niche position and niche specialization with climatic data [13], despite considerable interest in related (...truncated)