The origins of Neotropical amphibian biodiversity John J. Wiens Department of Ecology and Evolution Stony Brook University Stony Brook, New York, U.S.A

Why is biodiversity higher in the tropics? From Global Amphibian Assessment (2004) Global Patterns of Amphibian Diversity

from Francis and Currie (2003; Am. Nat.) Patterns of species richness “What environmental variables are correlated with high species richness?” Variables typically climatic (temperature, rainfall) or closely related (energy, productivity)

Patterns of species richness Environmental variables alone cannot directly explain patterns of species richness Ultimately, species richness patterns must be explained by processes that directly change number of species

Speciation (add species to region) Extinction (subtract species from region) Dispersal (add species to region) (subtract species from region) Number of species in region

Speciation Extinction Tropical Regions Temperate Regions Speciation Extinction Dispersal Underlying causes of high tropical diversity

Speciation Extinction Tropical Regions Temperate Regions Speciation Extinction Dispersal Climate and related factors

Why more species in the tropics? Two general explanations: 1) Diverse clades originate in tropics, disperse to temperate zone recently and infrequently, leaving less time for speciation to build up richness in temperate zone 2) Faster rate of diversification (speciation - extinction) in tropical clades (e.g., rapid tropical speciation, more temperate extinction)

Speciation Extinction Tropical Regions Temperate Regions Speciation Extinction dispersal Climate limits dispersal from tropical to temperate regions If clade originates in tropics, can have more tropical richness through more time for speciation, not differences in rates of speciation and extinction between regions

Speciation Extinction Tropical Regions Temperate Regions Speciation Extinction Dispersal Tropical environmental conditions lead to more speciation or less extinction (higher diversification rate)

Two stories about tropical diversity in amphibians What explains patterns of local species richness? (Causes of local richness patterns in treefrogs, Hylidae) For clades that show faster tropical diversification, what is it about tropical environments that causes this pattern? (Correlates of high diversification in salamanders, Plethodontidae)

Treefrogs (family Hylidae)

Santa Cecilia, Ecuador= 36 Cuzco Amazonico, Peru = 31 Boriacea, Brazil = 26 Savannah River Ecology Lab = 12 La Selva, Cost Rica = 12 Palenque, Ecuador = 10 Phylogenies becoming used to study large-scale richness patterns and local community structure, but not local richness Hylids show extreme variation in local diversity with more species in some sites in Amazonia than in all of Europe and Asia Hylid diversity correlates with overall anuran diversity Hylid Local Diversity

Built new, time calibrated phylogeny for ~362 hylid species (with BEAST) Obtained data on local diversity and climate for 123 sites (but focused on 12 localities representing major regions) What explains local diversity? (climate? time? traits?) Do sympatric clades constrain each other’s diversification? Hylid Local Diversity

Santa Cecilia, Ecuador= 36 Cuzco Amazonico, Peru = 31 Boriacea, Brazil = 26 Savannah River Ecology Lab = 12 La Selva, Cost Rica = 12 Palenque, Ecuador = 10 Hylid Local Diversity Weak relationships between local diversity and climate across regions Wiens, Pyron, and Moen (Ecol. Lett. in revision) r 2 = P = 0.04 r 2 = P = 0.30

Wiens, Pyron, and Moen (Ecol. Lett. in revision) Hylid Local Diversity Strong relationship between local diversity and how long clades have been present in region (using LAGRANGE) r 2 = P = 0.001

Higher local diversity in allopatric clades P = 0.04 Higher diversification rate in allopatric clades

Hylid Local Diversity Range of species body sizes is greater in more diverse communities (in the tropics) High local diversity associated with many species in same body size classes r 2 = P < Wiens, Pyron, and Moen (Ecol. Lett. in revision) Rates of body-size evolution are higher in allopatric clades (P = 0.04)

Treefrog Implications Time (and phylogeny) are important in explaining patterns of local-scale species richness, including high local diversity of Amazonia Sympatry between clades may slow rate of species diversification, but does not prevent accumulation of species richness over time Similarly, species interactions (clade sympatry) slows rate of body-size evolution, but does not prevent co- existence of species withi similar body size

Two stories about tropical diversity in amphibians What explains patterns of local species richness? (Causes of local richness patterns in treefrogs, Hylidae) For clades that show faster tropical diversification, what is it about tropical environments that causes this pattern? (Correlates of high diversification in salamanders, Plethodontidae)

Frogs and Tropical Diversification Many basal anuran families primarily temperate (e.g., ascaphids, discoglossids, pelobatids) Most anurans (96%) belong to single clade (Neobatrachia) centered in tropical regions Global diversity patterns dominated by higher diversification rate in tropics? Pipoidea (31 species) Ascaphidae (6 species) Discoglossoidea (22 species) Pelobatoidea (145 species) Neobatrachia (5,149 species) Temperate ascaphidTropical dendrobatid

Sooglossidae Ascaphidae Pipoidea Bombinatoridae Ranoidea Heleophrynidae Pelobatoidea 0 Millions of years ago Anurans Reconstructed phylogeny and divergence dates RAG-1 data for 84 species (almost all families) Penalized likelihood analysis (10 fossil calibration points) Estimated diversification rates for 15 clades temperate tropical Hyloidea Discoglossidae Megophryidae Caudiverbera Myobatrachidae Leiopelmatidae Neobatrachia Wiens (2007, Am. Nat.)

Diversification rate and latitude Strong relationship between diversification rate and latitude in anurans Wiens (2007, Am. Nat.)

9 of 10 salamander families primarily temperate One clade in one subfamily (bolitoglossine plethodontids) is tropical--but contains nearly half of all salamander species Global diversity patterns dominated by higher diversification rate in tropics? Diversification rate = speciation - extinction Temperate ambystomatid Tropical plethodontid Salamanders and Tropical Diversification

Tropical bolitoglossines Salamandridae Cryptobranchidae “Hynobiidae” Dicamptodontidae Proteidae Amphiumidae Ambystomatidae Plethodontidae Sirenidae Rhyacotritonidae 0 Millions of years ago Salamanders Reconstructed phylogeny and divergence dates RAG-1 data for 66 species (all families) Penalized likelihood analysis (11 fossil calibration points) Estimated diversification rates for 12 clades temperate tropical Wiens (2007, Am. Nat.)

Diversification rate and latitude Strong relationship between diversification rate and latitude in salamanders Wiens (2007, Am. Nat.)

Why are diversification rates higher in tropical clades? Many studies have shown faster diversification rates in tropical clades, including studies in butterflies (Cardillo et al. 2005), birds (Ricklefs 2006), and plants (Jansson & Davies 2008; Svenning et al. 2008) Little known about why tropical clades have faster rates (many hypotheses, few empirical tests) We used plethodontid salamanders as model system to address the “why”

Why are diversification rates higher in tropical clades? Built time-calibrated phylogeny for 250 plethodontid species Obtained GIS-based climatic data for all 250 species, did PCA on 19 climatic variables, used PCs 1–3 Divided into 15 clades, estimated rates of diversification and climatic- niche evolution (with Brownie) for each clade Kozak and Wiens (2010, Ecol. Lett.) Neotropics E North Am. W North Am.

Why are diversification rates higher in tropical clades? Strong relationship between rate of climatic-niche evolution and rate of diversification Tropical clades have higher rates of diversification and higher rates of climatic-niche evolution Clades that are geographically isolated have higher rates of niche evolution (e.g., subgenus Eladinea of Bolitoglossa, only radiation in Andes) Kozak and Wiens (2010, Ecol. Lett.) From PGLS, P = 0.008

Salamander Implications In plethodontids, high tropical diversification rates are associated with high rates of climatic-niche evolution, not particular climatic conditions Limited temperature seasonality in tropics may lead to greater climatic differences between species at different elevations (Janzen 1967) Faster rate of climatic niche evolution in isolated clades suggests that species interactions are important in driving niche conservatism

Climatic Niche Conservatism Climatic niche conservatism: retention of similar climatic distributions over time, may be relevant to: Adaptation (or not) to global warming Distribution of invasive species Allopatric speciation Large-scale biogeography of clades (and species richness) Spread of human agricultural species (and human history)

Why is biodiversity higher in the tropics? From Global Amphibian Assessment (2004) Global Patterns of Amphibian Diversity Conclusions: Both time and rates of diversification are important in explaining high tropical diversity (but at different scales) Relationship between causes of diversity and climate is not simple Species interactions are important, but in constraining evolutionary change, not driving it

Main Collaborators Hylid local diversity: Alex Pyron, Dan Moen Climatic niches and diversification: Ken Kozak Acknowledgments Funding National Science Foundation: AToL, Systematic Biology

Gracias! Obrigado! Thank you!