Fernanda P. Werneck

DEEP DIVERSIFICATION AND LONG-TERM PERSISTENCE IN THE SOUTH AMERICAN 'DRY DIAGONAL': INTEGRATING CONTINENT-WIDE PHYLOGEOGRAPHY AND DISTRIBUTION MODELING OF GECKOS

The relative influence of Neogene geomorphological events and Quaternary climatic changes as causal mechanisms on Neotropical diversification remains largely speculative, as most divergence timing inferences are based on a single locus and have limited taxonomic or geographic sampling. To investigate these influences, we use a multilocus (two mitochondrial and 11 nuclear genes) range‐wide sampling of Phyllopezus pollicaris, a gecko complex widely distributed across the poorly studied South American ‘dry diagonal’ biomes. Our approach couples traditional and model‐based phylogeography with geospatial methods, and demonstrates Miocene diversification and limited influence of Pleistocene climatic fluctuations on P. pollicaris. Phylogeographic structure and distribution models highlight that persistence across multiple isolated regions shaped the diversification of this species complex. Approximate Bayesian computation supports hypotheses of allopatric and ecological/sympatric speciation between lineages that largely coincide with genetic clusters associated with Chaco, Cerrado, and Caatinga, standing for complex diversification between the ‘dry diagonal’ biomes. We recover extremely high genetic diversity and suggest that eight well‐supported clades may be valid species, with direct implications for taxonomy and conservation assessments. These patterns exemplify how low‐vagility species complexes, characterized by strong genetic structure and pre‐Pleistocene divergence histories, represent ideal radiations to investigate broad biogeographic histories of associated biomes.

Phylogeny and cryptic diversity in geckos (Phyllopezus; Phyllodactylidae; Gekkota) from South America's open biomes

The gecko genus Phyllopezus occurs across South Americas open biomes: Cerrado, Seasonally Dry Tropical Forests (SDTF, including Caatinga), and Chaco. We generated a multi-gene dataset and estimated phylogenetic relationships among described Phyllopezus taxa and related species. We included exemplars from both described Phyllopezus pollicaris subspecies, P. p. pollicaris and P. p.przewalskii. Phylogenies from the concatenated data as well as species trees constructed from individual gene trees were largely congruent. All phylogeny reconstruction methods showed Bogertia lutzae as the sister species of Phyllopezus maranjonensis, rendering Phyllopezus paraphyletic. We synonymized the monotypic genus Bogertia with Phyllopezus to maintain a taxonomy that is isomorphic with phylogenetic history. We recovered multiple, deeply divergent, cryptic lineages within P. pollicaris. These cryptic lineages possessed mtDNA distances equivalent to distances among other gekkotan sister taxa. Described P. pollicaris subspecies are not reciprocally monophyletic and current subspecific taxonomy does not accurately reflect evolutionary relationships among cryptic lineages. We highlight the conservation significance of these results in light of the ongoing habitat loss in South Americas open biomes.

In the Wake of Invasion: Tracing the Historical Biogeography of the South American Cricetid Radiation (Rodentia, Sigmodontinae)

The Great American Biotic Interchange (GABI) was greatly influenced by the completion of the Isthmus of Panama and impacted the composition of modern faunal assemblages in the Americas. However, the contribution of preceding events has been comparatively less explored, even though early immigrants in the fossil records are evidence for waif dispersals. The cricetid rodents of the subfamily Sigmodontinae are a classic example of a species-rich South American radiation resulting from an early episode of North American invasion. Here, we provide a temporal and spatial framework to address key aspects of the historical biogeography and diversification of this diverse mammal group by using mitochondrial and nuclear DNA datasets coupled with methods of divergence time estimation, ancestral area reconstruction and comparative phylogenetics. Relaxed-clock time estimates indicate that divergence of the Sigmodontinae began in the middle–late Miocene (ca. 12–9 Ma). Dispersal-vicariance analyses point to the arrival of a single lineage of northern invaders with a widespread ancestral distribution and imply that the initial differentiation between Central and South America gave rise to the most basal groups within the subfamily. These two major clades diversified in the late Miocene followed by the radiation of main tribes until the early Pliocene. Within the Oryzomyalia, tribes diverged initially in eastern South America whereas multiple dispersals into the Andes promoted further diversification of the majority of modern genera. A comparatively uniform background tempo of diversification explains the species richness of sigmodontines across most nodes, except for two akodontine genera with recent increases in diversification rates. The bridging of the Central American seaway and episodes of low sea levels likely facilitated the invasion of South America long before the onset of the post-Isthmian phase of the GABI.

Biogeographic history and cryptic diversity of saxicolous Tropiduridae lizards endemic to the semiarid Caatinga.

BackgroundPhylogeographic research has advanced in South America, with increasing efforts on taxa from the dry diagonal biomes. However, the diversification of endemic fauna from the semiarid Caatinga biome in northeastern Brazil is still poorly known. Here we targeted saxicolous lizards of the Tropidurus semitaeniatus species group to better understand the evolutionary history of these endemic taxa and the Caatinga. We estimated a time-calibrated phylogeny for the species group based on two mitochondrial and two nuclear genes and jointly estimated the species limits and species tree within the group. We also devoted a denser phylogeographic sampling of the T. semitaeniatus complex to explore migration patterns, and the spatiotemporal diffusion history to verify a possible role of the São Francisco River as a promoter of differentiation in this saxicolous group of lizards.ResultsPhylogenetic analysis detected high cryptic genetic diversity, occurrence of unique microendemic lineages associated with older highlands, and a speciation history that took place during the Pliocene-Pleistocene transition. Species delimitation detected five evolutionary entities within the T. semitaeniatus species group, albeit with low support. Thus, additional data are needed for a more accurate definition of species limits and interspecific relationships within this group. Spatiotemporal analyses reconstructed the geographic origin of the T. semitaeniatus species complex to be located north of the present-day course of the São Francisco River, followed by dispersal that expanded its distribution towards the northwest and south. Gene flow estimates showed higher migration rates into the lineages located north of the São Francisco River.ConclusionsThe phylogenetic and population structures are intrinsically associated with stable rock surfaces and landscape rearrangements, such as the establishment of drainage basins located to the northern and southern distribution ranges. The T. semitaeniatus complex preserved high genetic diversity during range expansion, possibly as a result of frequent long-distance dispersal events. Our results indicate that both the current course of the São Francisco River and its paleo-courses had an important role in promoting diversification of the Caatinga endemic T. semitaeniatus species group.

Phylogeny, biogeography and evolution of clutch size in South American lizards of the genus Kentropyx (Squamata: Teiidae)

The lizard genus Kentropyx (Squamata: Teiidae) comprises nine species, which have been placed in three species groups (calcarata group, associated to forests ecosystems; paulensis and striata groups, associated to open ecosystems). We reconstructed phylogenetic relationships of Kentropyx based on morphology (pholidosis and coloration) and mitochondrial DNA data (12S and 16S), using maximum parsimony and Bayesian methods, and evaluated biogeographic scenarios based on ancestral areas analyses and molecular dating by Bayesian methods. Additionally, we tested the life‐history hypothesis that species of Kentropyx inhabiting open ecosystems (under seasonal environments) produce larger clutches with smaller eggs and that species inhabiting forest ecosystems (under aseasonal conditions) produce clutches with fewer and larger eggs, using Stearns’ phylogenetic‐subtraction method and canonical phylogenetic ordination to take in to account the effects of phylogeny. Our results showed that Kentropyx comprises three monophyletic groups, with K. striata occupying a basal position in opposition to previous suggestions of relationships. Additionally, Bayesian analysis of divergence time showed that Kentropyx may have originated at the Tertiary (Eocene/Oligocene) and the ‘Pleistocene Refuge Hypothesis’ may not explain the species diversification. Based on ancestral reconstruction and molecular dating, we argued that a savanna ancestor is more likely and that historical events during the Tertiary of South America promoted the differentiation of the genus, coupled with recent Quaternary events that were important as dispersion routes and for the diversification at populational levels. Clutch size and egg volume were not significantly different between major clades and ecosystems of occurrence, even accounting for the phylogenetic effects. Finally, we argue that phylogenetic constraints and phylogenetic inertia might be playing essential roles in life history evolution of Kentropyx.

Quaternary range and demographic expansion of Liolaemus darwinii (Squamata: Liolaemidae) in the Monte Desert of Central Argentina using Bayesian phylogeography and ecological niche modelling

Until recently, most phylogeographic approaches have been unable to distinguish between demographic and range expansion processes, making it difficult to test for the possibility of range expansion without population growth and vice versa. In this study, we applied a Bayesian phylogeographic approach to reconstruct both demographic and range expansion in the lizard Liolaemus darwinii of the Monte Desert in Central Argentina, during the Late Quaternary. Based on analysis of 14 anonymous nuclear loci and the cytochrome b mitochondrial DNA gene, we detected signals of demographic expansion starting at ~55 ka based on Bayesian Skyline and Skyride Plots. In contrast, Bayesian relaxed models of spatial diffusion suggested that range expansion occurred only between ~95 and 55 ka, and more recently, diffusion rates were very low during demographic expansion. The possibility of population growth without substantial range expansion could account for the shared patterns of demographic expansion during the Last Glacial Maxima (OIS 2 and 4) in fish, small mammals and other lizards of the Monte Desert. We found substantial variation in diffusion rates over time, and very high rates during the range expansion phase, consistent with a rapidly advancing expansion front towards the southeast shown by palaeo‐distribution models. Furthermore, the estimated diffusion rates are congruent with observed dispersal rates of lizards in field conditions and therefore provide additional confidence to the temporal scale of inferred phylogeographic patterns. Our study highlights how the integration of phylogeography with palaeo‐distribution models can shed light on both demographic and range expansion processes and their potential causes.

Reproduction, Body Size, and Diet of Polychrus acutirostris (Squamata: Polychrotidae) in Two Contrasting Environments in Brazil

Abstract We compared reproduction, diet, and body size of Polychrus acutirostris (Squamata: Polychrotidae) from the Cerrado and Caatinga biomes in Brazil. Because these two biomes have widely different climates, we predicted that lizards in Caatinga would produce smaller clutches in response to rainfall unpredictability. We also expected reproductive timing to differ between biomes, with lizards occurring in the Cerrado producing a single clutch in association with the predictable rains of October–November. Contrary to expectations, clutches had fewer (although larger) eggs in Cerrado. Reproductive period was remarkably similar (peak of female reproductive activity in November), but female reproduction started 1 month earlier in Cerrado. Diet composition was also similar, with the exception of spiders, that exhibited a high index of relative importance in Cerrado but were nearly absent in Caatinga lizard diets. Lizards from both biomes ingested a large proportion of plant material, as well as soft-bodied arboreal arthropods, such as orthopterans, and mostly slow-moving, large arboreal insects. Rainfall predictability in the Cerrado therefore did not influence Polychrus reproduction or diet in the same manner as in other lizard species. The large number of small eggs in the Caatinga suggests that the competitive environment for offspring is either unpredictable or that mortality is high but random. Rain forest Polychrus lizards produce few large eggs, suggesting that the competitive environment for offspring is predictably intense and mortality is non-random. Cerrado Polychrus lizards seem intermediate between Caatinga and rain forest Polychrus lizards, producing fewer and larger eggs than their conspecifics in the Caatinga but relatively more and smaller eggs than rain forest Polychrus species.

Cryptic lineages and diversification of an endemic anole lizard (Squamata, Dactyloidae) of the Cerrado hotspot ☆ ☆☆

The Cerrado is a wide Neotropical savanna with tremendously high endemic diversity. Yet, it is not clear what the prevalent processes leading to such diversification are. We used the Cerrado-endemic lizard Norops meridionalis to investigate the main abiotic factors that promoted genetic divergence, the timings of these divergence events, and how these relate to cryptic diversity in the group. We sequenced mitochondrial and nuclear genes from 21 sites of N. meridionalis to generate species tree, divergence time estimations, and estimate species limits. We also performed population-level analysis and estimated distribution models to test the roles of niche conservatism and divergence in the group diversification. We found that N. meridionalis is composed by at least five cryptic species. Divergence time estimations suggest that the deepest branches split back into the early-mid Miocene, when most of the geophysical activity of the Cerrado took place. The deep divergences found in N. meridionalis suggest that beta anoles invaded South America much earlier than previously thought. Recent published evidence supports this view, indicating that the Panama gap closed as early as 15 mya, allowing for an early invasion of Norops into South America. The spatial pattern of diversification within N. meridionalis follows a northwest-southeast direction, which is consistent across several species of vertebrates endemic to the Cerrado. Also, we found evidence for non-stationary isolation by distance, which occurs when genetic differentiation depends on space. Our preliminary data in two out of five lineages suggest that niche conservatism is an important mechanism that promoted geographic fragmentation in the group.

Estimating synchronous demographic changes across populations using hABC, and its application for a herpetological community from Northeastern Brazil

Many studies propose that Quaternary climatic cycles contracted and/or expanded the ranges of species and biomes. Strong expansion–contraction dynamics of biomes presume concerted demographic changes of associated fauna. The analysis of temporal concordance of demographic changes can be used to test the influence of Quaternary climate on diversification processes. Hierarchical approximate Bayesian computation (hABC) is a powerful and flexible approach that models genetic data from multiple species, and can be used to estimate the temporal concordance of demographic processes. Using available single‐locus data, we can now perform large‐scale analyses, both in terms of number of species and geographic scope. Here, we first compared the power of four alternative hABC models for a collection of single‐locus data. We found that the model incorporating an a priori hypothesis about the timing of simultaneous demographic change had the best performance. Second, we applied the hABC models to a data set of seven squamate and four amphibian species occurring in the Seasonally Dry Tropical Forests (Caatinga) in northeastern Brazil, which, according to paleoclimatic evidence, experienced an increase in aridity during the Pleistocene. If this increase was important for the diversification of associated xeric‐adapted species, simultaneous population expansions should be evident at the community level. We found a strong signal of synchronous population expansion in the Late Pleistocene, supporting the increase of the Caatinga during this time. This expansion likely enhanced the formation of communities adapted to high aridity and seasonality and caused regional extirpation of taxa adapted to wet forest.

Ecological and historical views of the diversification of Geositta miners (Aves: Furnariidae: Sclerurinae)

Diverse historical and ecological factors determine and drive diversification of vertebrate lineages. Historical factors (e.g., orogenic movements) are expected to act on coarser spatial and temporal scales than contemporary ecological factors (e.g., climate and biotic interactions). However, distinctions between such scales remain arbitrary, and yet are important to understanding which factors acted in the emergence of new species. We inferred ancestral states for climatic niches on ecological scales, and ancestral area reconstructions for the genus Geositta on deeper time scales. Ecological niches did not overlap more between sister species than among more distant relatives, and rather pointed to a plastic scenario for climatic diversification of Geositta rather than niche conservatism. Events temporally associated with the formation of the Andes (Miocene) seem to explain most of the diversification. In sum, climatic factors may not have had a great influence in the diversification of Geositta, at least in the context of Pleistocene climate fluctuations.ZusammenfassungÖkologische und historische Betrachtung der Diversifikation vonGeosittaErdhackern (Töpfervögel: Sclerurinae) Es gibt eine Anzahl historischer und ökologischer Faktoren, die die Diversifikation der Abstammungslinien von Wirbeltieren bestimmen und voranbringen. Historische Faktoren wie z.B. topographische Veränderungen durch Gebirgsbildung wirken sich sicherlich eher in einem gröberen zeitlichen und räumlichen Rahmen aus als zeitnähere ökologische Faktoren wie z.B. klimatologische und biotische Wechselwirkungen. Zwar sind derartige Unterscheidungen nach Größenordnungen willkürlich gewählt, sie sind aber dennoch wichtig für das Verständnis, welche Faktoren bei der Entstehung neuer Arten eine Rolle gespielt haben könnten. Für die Abstammungslinien der Gattung Geositta zogen wir Rückschlüsse zum einen auf einer ökologischen Zeitskala, für klimatologische Nischen, wie auch auf einer weiter zurückreichenden Zeitskala durch eine Rekonstruktion früherer, angestammter Siedlungsgebiete. Die ökologischen Nischen überlappten zwischen Schwesternarten nicht stärker als zwischen entfernteren Arten und wiesen bei der klimatischen Diversifikation von Geositta eher auf eine gewisse Plastizität als auf eine Nischen-Konstanz hin. Ereignisse, die zeitlich mit der Entstehung der Anden (Miozän) zusammenfallen, scheinen den Großteil der Diversifikation erklären zu können. Zusammenfassend kann gesagt werden, dass in der Diversifikation von Geositta klimatische Faktoren vermutlich keine große Rolle gespielt haben, zumindest während der im Pleistozän aufgetretenen Klimaveränderungen.