Patrick R. Stephens

Niche conservatism as an emerging principle in ecology and conservation biology.

The diversity of life is ultimately generated by evolution, and much attention has focused on the rapid evolution of ecological traits. Yet, the tendency for many ecological traits to instead remain similar over time [niche conservatism (NC)] has many consequences for the fundamental patterns and processes studied in ecology and conservation biology. Here, we describe the mounting evidence for the importance of NC to major topics in ecology (e.g. species richness, ecosystem function) and conservation (e.g. climate change, invasive species). We also review other areas where it may be important but has generally been overlooked, in both ecology (e.g. food webs, disease ecology, mutualistic interactions) and conservation (e.g. habitat modification). We summarize methods for testing for NC, and suggest that a commonly used and advocated method (involving a test for phylogenetic signal) is potentially problematic, and describe alternative approaches. We suggest that considering NC: (1) focuses attention on the within-species processes that cause traits to be conserved over time, (2) emphasizes connections between questions and research areas that are not obviously related (e.g. invasives, global warming, tropical richness), and (3) suggests new areas for research (e.g. why are some clades largely nocturnal? why do related species share diseases?).

Explaining Species Richness from Continents to Communities: The Time‐for‐Speciation Effect in Emydid Turtles

Speciation is the process that ultimately generates species richness. However, the time required for speciation to build up diversity in a region is rarely considered as an explanation for patterns of species richness. We explored this “time‐for‐speciation effect” on patterns of species richness in emydid turtles. Emydids show a striking pattern of high species richness in eastern North America (especially the southeast) and low diversity in other regions. At the continental scale, species richness is positively correlated with the amount of time emydids have been present and speciating in each region, with eastern North America being the ancestral region. Within eastern North America, higher regional species richness in the southeast is associated with smaller geographic range sizes and not greater local species richness in southern communities. We suggest that these patterns of geographic range size variation and local and regional species richness in eastern North America are caused by glaciation, allopatric speciation, and the time‐for‐speciation effect. We propose that allopatric speciation can simultaneously decrease geographic range size and increase regional diversity without increasing local diversity and that geographic range size can determine the relationship between α, β, and γ diversity. The time‐for‐speciation effect may act through a variety of processes at different spatial scales to determine diverse patterns of species richness.

Phylogeny, niche conservatism and the latitudinal diversity gradient in mammals

Biologists have long searched for mechanisms responsible for the increase in species richness with decreasing latitude. The strong correlation between species richness and climate is frequently interpreted as reflecting a causal link via processes linked to energy or evolutionary rates. Here, we investigate how the aggregation of clades, as dictated by phylogeny, can give rise to significant climate–richness gradients without gradients in diversification or environmental carrying capacity. The relationship between climate and species richness varies considerably between clades, regions and time periods in a global-scale phylogenetically informed analysis of all terrestrial mammal species. Many young clades show negative richness–temperature slopes (more species at cooler temperatures), with the ages of these clades coinciding with the expansion of temperate climate zones in the late Eocene. In carnivores, we find steeply positive richness–temperature slopes in clades with restricted distributions and tropical origins (e.g. cat clade), whereas widespread, temperate clades exhibit shallow, negative slopes (e.g. dog–bear clade). We show that the slope of the global climate–richness gradient in mammals is driven by aggregating Chiroptera (bats) with their Eutherian sister group. Our findings indicate that the evolutionary history should be accounted for as part of any search for causal links between environment and species richness.

The Evolution of Maximum Body Size of Terrestrial Mammals

How Mammals Grew in Size Mammals diversified greatly after the end-Cretaceous extinction, which eliminated the dominant land animals (dinosaurs). Smith et al. (p. 1216) examined how the maximum size of mammals increased during their radiation in each continent. Overall, mammal size increased rapidly, then leveled off after about 25 million years. This pattern holds true on most of the continents—even though data are sparse for South America—and implies that mammals grew to fill available niches before other environmental and biological limits took hold. Maximum mammal size increased at the beginning of the Cenozoic, then leveled off after about 25 million years. The extinction of dinosaurs at the Cretaceous/Paleogene (K/Pg) boundary was the seminal event that opened the door for the subsequent diversification of terrestrial mammals. Our compilation of maximum body size at the ordinal level by sub-epoch shows a near-exponential increase after the K/Pg. On each continent, the maximum size of mammals leveled off after 40 million years ago and thereafter remained approximately constant. There was remarkable congruence in the rate, trajectory, and upper limit across continents, orders, and trophic guilds, despite differences in geological and climatic history, turnover of lineages, and ecological variation. Our analysis suggests that although the primary driver for the evolution of giant mammals was diversification to fill ecological niches, environmental temperature and land area may have ultimately constrained the maximum size achieved.

Estimating the normal background rate of species extinction

A key measure of humanitys global impact is by how much it has increased species extinction rates. Familiar statements are that these are 100-1000 times pre-human or background extinction levels. Estimating recent rates is straightforward, but establishing a background rate for comparison is not. Previous researchers chose an approximate benchmark of 1 extinction per million species per year (E/MSY). We explored disparate lines of evidence that suggest a substantially lower estimate. Fossil data yield direct estimates of extinction rates, but they are temporally coarse, mostly limited to marine hard-bodied taxa, and generally involve genera not species. Based on these data, typical background loss is 0.01 genera per million genera per year. Molecular phylogenies are available for more taxa and ecosystems, but it is debated whether they can be used to estimate separately speciation and extinction rates. We selected data to address known concerns and used them to determine median extinction estimates from statistical distributions of probable values for terrestrial plants and animals. We then created simulations to explore effects of violating model assumptions. Finally, we compiled estimates of diversification-the difference between speciation and extinction rates for different taxa. Median estimates of extinction rates ranged from 0.023 to 0.135 E/MSY. Simulation results suggested over- and under-estimation of extinction from individual phylogenies partially canceled each other out when large sets of phylogenies were analyzed. There was no evidence for recent and widespread pre-human overall declines in diversity. This implies that average extinction rates are less than average diversification rates. Median diversification rates were 0.05-0.2 new species per million species per year. On the basis of these results, we concluded that typical rates of background extinction may be closer to 0.1 E/MSY. Thus, current extinction rates are 1,000 times higher than natural background rates of extinction and future rates are likely to be 10,000 times higher.

Replicate patterns of species richness, historical biogeography, and phylogeny in Holarctic treefrogs.

Abstract In recent decades, the field of historical biogeography has become increasingly divorced from evolutionary biology, ecology, and studies of species richness. In this paper, we explore the evolutionary causes of patterns of biogeography and species richness in Northern Hemisphere treefrogs, combining phylogenetics, ancestral area reconstruction, molecular dating methods, and ecological niche modeling. We reconstructed phylogenetic relationships among 58 hylid taxa using data from two mitochondrial genes (12S, ND1) and two nuclear genes (POMC, c‐myc). We find that parallel patterns of species richness have developed in Europe, Asia, and in two separate clades of North American hylids, with the highest richness at midtemperate latitudes (30–35d̀) on each continent. This pattern is surprising given that hylids overall show higher species richness in the New World tropics and given many standard ecological explanations for the latitudinal diversity gradient (e.g., energy, productivity, mid‐domain effect). The replicate pattern in Holarctic hylids seems to reflect specialized tolerance for temperate climate regimes or possibly the effects of competition. The results also suggest that long‐range dispersal between continental regions with similar climatic regimes may be easier than dispersal between geographically adjacent regions with different climatic regimes. Our results show the importance of ecology and evolution to large‐scale biogeography and the importance of largescale biogeography to understanding patterns of species richness.

EVOLUTION OF SEXUAL SIZE DIMORPHISMS IN EMYDID TURTLES: ECOLOGICAL DIMORPHISM, RENSCH'S RULE, AND SYMPATRIC DIVERGENCE

The origin of sexual size dimorphisms (SSD) has long been a central topic in evolutionary biology. However, there is little agreement as to which factors are most important in driving the evolution of SSD, and several hypotheses concerning SSD evolution have never been tested empirically. Emydid turtles include species with both male and female-biased SSD, and some emydids exhibit among the most extreme SSD in tetrapods. Here, we use a comparative phylogenetic approach in emydids to analyze the origins of SSD and test several hypotheses for the evolution of SSD, some for the first time. We test the Fairbairn-Preziosi hypothesis for the origin of Renschs rule, and support it in lineages with male-biased SSD but not those with female-biased SSD. We also find support for the secondary ecological dimorphism hypothesis, which proposes that selection for ecological divergence between sexes exaggerates preexisting SSD. Finally, we find only equivocal support for the Bolnick-Doebeli hypothesis, which relates intersexual ecological divergence to interspecific ecological divergence. Our results also illustrate how global analyses of SSD may mislead in groups in which the factors that drive the evolution of SSD vary among clades.

The maximum rate of mammal evolution

How fast can a mammal evolve from the size of a mouse to the size of an elephant? Achieving such a large transformation calls for major biological reorganization. Thus, the speed at which this occurs has important implications for extensive faunal changes, including adaptive radiations and recovery from mass extinctions. To quantify the pace of large-scale evolution we developed a metric, clade maximum rate, which represents the maximum evolutionary rate of a trait within a clade. We applied this metric to body mass evolution in mammals over the last 70 million years, during which multiple large evolutionary transitions occurred in oceans and on continents and islands. Our computations suggest that it took a minimum of 1.6, 5.1, and 10 million generations for terrestrial mammal mass to increase 100-, and 1,000-, and 5,000-fold, respectively. Values for whales were down to half the length (i.e., 1.1, 3, and 5 million generations), perhaps due to the reduced mechanical constraints of living in an aquatic environment. When differences in generation time are considered, we find an exponential increase in maximum mammal body mass during the 35 million years following the Cretaceous–Paleogene (K–Pg) extinction event. Our results also indicate a basic asymmetry in macroevolution: very large decreases (such as extreme insular dwarfism) can happen at more than 10 times the rate of increases. Our findings allow more rigorous comparisons of microevolutionary and macroevolutionary patterns and processes.

Bridging the gap between community ecology and historical biogeography: niche conservatism and community structure in emydid turtles

Historical (phylogenetic) biogeography and community ecology were once integrated as part of the broader study of organismal diversity, but in recent decades have become largely separate disciplines. This is unfortunate because many patterns studied by community ecologists may originate through processes studied by historical biogeographers and vice versa. In this study, we explore the causes of a geographic pattern of community structure (habitat use) in the emydid turtle assemblages of eastern North America, with more semi‐terrestrial species of the subfamily Emydinae in the north and more aquatic species of Deirochelyinae in the south. Specifically, we address the factors that prevent northern emydines from invading southern communities. We test for competitive exclusion by examining patterns of range overlap, and test for the role of niche conservatism using analyses of climatic and physiological data based on a multilocus molecular phylogeny. We find no support for competitive exclusion, whereas several lines of evidence support the idea that niche conservatism has prevented northern emydines from dispersing into southern communities. Our results show how understanding the causes of patterns of historical biogeography may help explain patterns of community structure.

Phylogeny meets ecotoxicology: evolutionary patterns of sensitivity to a common insecticide

Pesticides commonly occur in aquatic systems and pose a substantial challenge to the conservation of many taxa. Ecotoxicology has traditionally met this challenge by focusing on short‐term, single‐species tests and conducting risk assessments based on the most sensitive species tested. Rarely have ecotoxicology data been examined from an evolutionary perspective, and to our knowledge, there has never been a phylogenetic analysis of sensitivity, despite the fact that doing so would provide insights into patterns of sensitivity among species and identify which clades are the most sensitive to a particular pesticide. We examined phylogenetic patterns of pesticide sensitivity in amphibians, a group of conservation concern owing to global population declines. Using the insecticide endosulfan, we combined previously published results across seven species of tadpoles and added eight additional species from the families Bufonidae, Hylidae, and Ranidae. We found significant phylogenetic signal in the sensitivity to the insecticide and in the existence of time lag effects on tadpole mortality. Bufonids were less sensitive than hylids, which were less sensitive than the ranids. Moreover, mortality time lags were common in ranids, occasional in hylids, and rare in bufonids. These results highlight the importance of an evolutionary perspective and offer important insights for conservation.