Climate change, extinction, and Sky Island biogeography in a montane lizard.

Around the world, many species are confined to "Sky Islands," with different populations in isolated patches of montane habitat. How does this pattern arise? One scenario is that montane species were widespread in lowlands when climates were cooler, and were isolated by local extinction caused by warming conditions. This scenario implies that many montane species may be highly susceptible to anthropogenic warming. Here, we test this scenario in a montane lizard (Sceloporus jarrovii) from the Madrean Sky Islands of southeastern Arizona. We combined data from field surveys, climate, population genomics, and physiology. Overall, our results support the hypothesis that this species' current distribution is explained by local extinction caused by past climate change. However, our results for this species differ from simple expectations in several ways: (a) their absence at lower elevations is related to warm winter temperatures, not hot summer temperatures; (b) they appear to exclude a low-elevation congener from higher elevations, not the converse; (c) they are apparently absent from many climatically suitable but low mountain ranges, seemingly "pushed off the top" by climates even warmer than those today; (d) despite the potential for dispersal among ranges during recent glacial periods (~18,000 years ago), populations in different ranges diverged ~4.5-0.5 million years ago and remained largely distinct; and (e) body temperatures are inversely related to climatic temperatures among sites. These results may have implications for many other Sky Island systems. More broadly, we suggest that Sky Island species may be relevant for predicting responses to future warming.

Inferring introgression using RADseq and DFOIL : Power and pitfalls revealed in a case study of spiny lizards (Sceloporus).

Introgression is now commonly reported in studies across the Tree of Life, aided by recent advancements in data collection and analysis. Nevertheless, researchers working with nonmodel species lacking reference genomes may be stymied by a mismatch between available resources and methodological demands. In this study, we demonstrate a fast and simple approach for inferring introgression using RADseq data, and apply it to a case study involving spiny lizards (Sceloporus) from northeastern México. First, we find evidence for recurrent mtDNA introgression between the two focal species based on patterns of mito-nuclear discordance. We then test for nuclear introgression by exhaustively applying the "five-taxon" D-statistic (DFOIL ) to all relevant individuals sampled for RADseq data. In our case, this exhaustive approach (dubbed "ExDFOIL ") entails testing up to ~250,000 unique four-taxon combinations of individuals across species. To facilitate use of this ExDFOIL approach, we provide scripts for many relevant tasks, including the selection of appropriate four-taxon combinations, execution of DFOIL tests in parallel and visualization of introgression results in phylogenetic and geographic space. Using ExDFOIL , we find evidence for ancient introgression between the focal species. Furthermore, we reveal geographic variation in patterns of introgression that is consistent with patterns of mito-nuclear discordance and with recurrent introgression. Overall, our study demonstrates that the combination of DFOIL and RADseq data can effectively detect introgression under a variety of sampling conditions (for individuals, populations and loci). Importantly, we also find evidence that batch-specific error and linkage in RADseq data may mislead inferences of introgression under certain conditions.

Molecular phylogeny and diversification of Malagasy bright-eyed tree frogs (Mantellidae: Boophis).

We investigate the molecular phylogeny of Boophis, a group of arboreal frogs from the Malagasy-Comoroan family Mantellidae. Based on newly acquired DNA sequences of five mitochondrial and five nuclear markers (7444 base pairs), we infer a phylogeny of Boophis with complete species-level taxon sampling. We reconstruct the phylogeny using Bayesian inference and maximum likelihood and estimate divergence dates for the major clades of the genus. The phylogenetic analyses together support the monophyly of the two subgenera (Sahona and Boophis), and provide strong support for most previously identified species groups, except that the B. ulftunni group is nested within the B. majori group. We also erect a new species group related to the B. mandraka group, the B. blommersae group, composed of small-sized, brown stream-breeding frogs previously included within the B. majori group. Finally, we use the resulting phylogeny to illustrate striking examples of repeated evolution of coloration and ventral transparency and address the biogeographic history and broad pattern of species diversification in the genus. Ancestral area reconstructions provide evidence that Boophis diversified within the Eastern highland forests of Madagascar, and we suggest that adaptation to these highland areas was important in their diversification.

Rapid Diversification and Time Explain Amphibian Richness at Different Scales in the Tropical Andes, Earth's Most Biodiverse Hotspot.

The Tropical Andes make up Earth's most species-rich biodiversity hotspot for both animals and plants. Nevertheless, the ecological and evolutionary processes underlying this extraordinary richness remain uncertain. Here, we examine the processes that generate high richness in the Tropical Andes relative to other regions in South America and across different elevations within the Andes, using frogs as a model system. We combine distributional data, a newly generated time-calibrated phylogeny for 2,318 frog species, and phylogenetic comparative methods to test the relative importance of diversification rates and colonization times for explaining Andean diversity at different scales. At larger scales (among regions and families), we find that faster diversification rates in Andean clades most likely explain high Andean richness. In contrast, at smaller temporal and spatial scales (within family-level clades within the Andes), diversification rates rarely explain richness patterns. Instead, we show that colonization times are important for shaping elevational richness patterns within the Andes, with more species found in habitats colonized earlier. We suggest that these scale-dependent patterns might apply to many other richness gradients. Recognition of this scale dependence may help to reconcile conflicting results among studies of richness patterns across habitats, regions, and organisms.

Discovery of a Giant Chameleon-Like Lizard (Anolis) on Hispaniola and Its Significance to Understanding Replicated Adaptive Radiations.

We report a new chameleon-like Anolis species from Hispaniola that is ecomorphologically similar to congeners found only on Cuba. Lizards from both clades possess short limbs and a short tail and utilize relatively narrow perches, leading us to recognize a novel example of ecomorphological matching among islands in the well-known Greater Antillean anole radiation. This discovery supports the hypothesis that the assembly of island faunas can be substantially deterministic and highlights the continued potential for basic discovery to reveal new insights in well-studied groups. Restricted to a threatened band of midelevation transitional forest near the border of the Dominican Republic and Haiti, this new species appears to be highly endangered.

A new species of bright-eyed treefrog (Mantellidae) from Madagascar, with comments on call evolution and patterns of syntopy in the Boophis ankaratra complex.

We describe a new species of Boophis treefrog from Ranomafana National Park in the southern central east of Madagascar. This region has remarkably high anuran diversity, and along with neighbouring sites, hosts more than 35 Boophis species. Boophis boppa sp. nov. is part of the B. ankaratra sub-clade (herein named the B. ankaratra complex), previously identified within the monophyletic B. albipunctatus species group. It occurs sympatrically with two other species of the complex (B. ankaratra and B. schuboeae). Morphological differentiation of species within the B. ankaratra clade remains elusive, but species are well characterized by distinct advertisement calls, with B. boppa having the longest note duration and inter-note intervals when compared to closely related species. Furthermore, it has moderate differentiation in mitochondrial DNA, with pairwise distances of 1.9-3.7% to all other species in sequences of the mitochondrial 16S rRNA marker. Additional evidence is given by the lack of haplotype sharing with related species for the nuclear exon DNAH-3. All examples of syntopic occurrence in this complex involve species with strongly different advertisement calls, while allopatric species have more similar calls. Such a pattern might result from adaptive call co-evolution but could also be the result of non-adaptive processes. Thorough clarification of the systematics of the B. ankaratra sub-clade is required, and we outline future directions for both bioacoustic and genetic research.

When do species-tree and concatenated estimates disagree? An empirical analysis with higher-level scincid lizard phylogeny.

Simulation studies suggest that coalescent-based species-tree methods are generally more accurate than concatenated analyses. However, these species-tree methods remain impractical for many large datasets. Thus, a critical but unresolved issue is when and why concatenated and coalescent species-tree estimates will differ. We predict such differences for branches in concatenated trees that are short, weakly supported, and have conflicting gene trees. We test these predictions in Scincidae, the largest lizard family, with data from 10 nuclear genes for 17 ingroup taxa and 44 genes for 12 taxa. We support our initial predictions, andsuggest that simply considering uncertainty in concatenated trees may sometimes encompass the differences between these methods. We also found that relaxed-clock concatenated trees can be surprisingly similar to the species-tree estimate. Remarkably, the coalescent species-tree estimates had slightly lower support values when based on many more genes (44 vs. 10) and a small (∼30%) reduction in taxon sampling. Thus, taxon sampling may be more important than gene sampling when applying species-tree methods to deep phylogenetic questions. Finally, our coalescent species-tree estimates tentatively support division of Scincidae into three monophyletic subfamilies, a result otherwise found only in concatenated analyses with extensive species sampling.

Evolution of paedomorphosis in plethodontid salamanders: ecological correlates and re-evolution of metamorphosis.

Life-history modes can profoundly impact the biology of a species, and a classic example is the dichotomy between metamorphic (biphasic) and paedomorphic (permanently aquatic) life-history strategies in salamanders. However, despite centuries of research on this system, several basic questions about the evolution of paedomorphosis in salamanders have not been addressed. Here, we use a nearly comprehensive, time-calibrated phylogeny of spelerpine plethodontids to reconstruct the evolution of paedomorphosis and to test if paedomorphosis is (1) reversible; (2) associated with living in caves; (3) associated with relatively dry climatic conditions on the surface; and (4) correlated with limited range size and geographic dispersal. We find that paedomorphosis arose multiple times in spelerpines. We also find evidence for re-evolution of metamorphosis after several million years of paedomorphosis in a lineage of Eurycea from the Edwards Plateau region of Texas. We also show for the first time using phylogenetic comparative methods that paedomorphosis is highly correlated with cave-dwelling, arid surface environments, and small geographic range sizes, providing insights into both the causes and consequences of this major life history transition.

Evolution of viviparity: a phylogenetic test of the cold-climate hypothesis in phrynosomatid lizards.

The evolution of viviparity is a key life-history transition in vertebrates, but the selective forces favoring its evolution are not fully understood. With >100 origins of viviparity, squamate reptiles (lizards and snakes) are ideal for addressing this issue. Some evidence from field and laboratory studies supports the "cold-climate" hypothesis, wherein viviparity provides an advantage in cold environments by allowing mothers to maintain higher temperatures for developing embryos. Surprisingly, the cold-climate hypothesis has not been tested using both climatic data and phylogenetic comparative methods. Here, we investigate the evolution of viviparity in the lizard family Phrynosomatidae using GIS-based environmental data, an extensive phylogeny (117 species), and recently developed comparative methods. We find significant relationships between viviparity and lower temperatures during the warmest (egg-laying) season, strongly supporting the cold-climate hypothesis. Remarkably, we also find that viviparity tends to evolve more frequently at tropical latitudes, despite its association with cooler climates. Our results help explain this and two related patterns that seemingly contradict the cold-climate hypothesis: the presence of viviparous species restricted to low-elevation tropical regions and the paucity of viviparous species at high latitudes. Finally, we examine whether viviparous taxa may be at higher risk of extinction from anthropogenic climate change.

Using genomic data to revisit an early example of reproductive character displacement in Haitian Anolis lizards.

The pattern of reproductive character displacement (RCD)-in which traits associated with reproductive isolation are more different where two species occur together than where they occur in isolation-is frequently attributed to reinforcement, a process during which natural selection acting against maladaptive mating events leads to enhanced prezygotic isolation between species or incipient species. One of the first studies of RCD to include molecular genetic data was described 40 years ago in a complex of Haitian trunk anole lizards using a small number of allozyme loci. In this example, Anolis caudalis appears to experience divergence in the color and pattern of an extensible throat fan, or dewlap, in areas of contact with closely related species at the northern and southern limits of its range. However, this case study has been largely overlooked for decades; meanwhile, explanations for geographic variation in dewlap color and pattern have focused primarily on adaptation to local signalling environments. We reinvestigate this example using amplified fragment length polymorphism (AFLP) genome scans, mtDNA sequence data, information on dewlap phenotypes and GIS data on environmental variation to test the hypothesis of RCD generated by reinforcement in Haitian trunk anoles. Together, our phenotypic and genetic results are consistent with RCD at the southern and northern limits of the range of A. caudalis. We evaluate the evidence for reinforcement as the explanation for RCD in Haitian trunk anoles, consider alternative explanations and provide suggestions for future work on the relationship between dewlap variation and speciation in Haitian trunk anoles.