The importance of the Andes in the evolutionary radiation of Sigmodontinae (Rodentia, Cricetidae), the most diverse group of mammals in the Neotropics.

The Andean mountains stand out for their striking species richness and endemicity that characterize many emblematic Neotropical clades distributed in or around these mountains. The radiation of the Sigmodontinae subfamily, the most diversified mammalian group in the Neotropics, has been historically related to Andean orogenesis. We aim to evaluate this interplay between geological processes and biological responses through the diversification dynamics, the biogeographical history, and the range evolution of the subfamily. For these, we built the most comprehensive phylogeny and gathered 14,836 occurrences for the subfamily. We identified one shift in the speciation rate in the genus Akodon, which suffered their Andean radiation after the arrival of non-Andean ancestors. Our biogeographic analyses show multiple dispersal paths throughout the evolution that allowed this subfamily to colonize all Neotropics. The Northern Andes and Central-Southern Andes were the most important sources of diversity. In addition, the Central-Southern Andes were the most relevant sink, receiving the highest number of lineages. The Andean region exhibited higher speciation and turnover rates than non-Andean regions. Thus, our results support the crucial role of the Andean Mountains in the Sigmodontinae radiation, acting as a "macroevolutionary cradle" and "species attractor" for several sigmodontine lineages at different times, and as a "species pump" becoming the biogeographic source of multiple widely distributed neotropical lineages. Then, complex macroevolutionary dynamics would explain these rodents' high extant Andean diversity and their wide distribution in the Neotropics.

The decoupled nature of basal metabolic rate and body temperature in endotherm evolution.

The origins of endothermy in birds and mammals are important events in vertebrate evolution. Endotherms can maintain their body temperature (Tb) over a wide range of ambient temperatures primarily using the heat that is generated continuously by their high basal metabolic rate (BMR)1. There is also an important positive feedback loop as Tb influences BMR1-3. Owing to this interplay between BMRs and Tb, many ecologists and evolutionary physiologists posit that the evolution of BMR and Tb must have been coupled during the radiation of endotherms3-5, changing with similar trends6-8. However, colder historical environments might have imposed strong selective pressures on BMR to compensate for increased rates of heat loss and to keep Tb constant9-12. Thus, adaptation to cold ambient temperatures through increases in BMR could have decoupled BMR from Tb and caused different evolutionary routes to the modern diversity in these traits. Here we show that BMR and Tb were decoupled in approximately 90% of mammalian phylogenetic branches and 36% of avian phylogenetic branches. Mammalian BMRs evolved with rapid bursts but without a long-term directional trend, whereas Tb evolved mostly at a constant rate and towards colder bodies from a warmer-bodied common ancestor. Avian BMRs evolved predominantly at a constant rate and without a long-term directional trend, whereas Tb evolved with much greater rate heterogeneity and with adaptive evolution towards colder bodies. Furthermore, rapid shifts that lead to both increases and decreases in BMRs were linked to abrupt changes towards colder ambient temperatures-although only in mammals. Our results suggest that natural selection effectively exploited the diversity in mammalian BMRs under diverse, often-adverse historical thermal environments.

Genetic variability and structure of the Olive Field Mouse: a sigmodontine rodent in a biodiversity hotspot of southern Chile.

The temperate rainforests of southern Chile, a recognized biodiversity hotspot, were significantly affected by Pleistocene glacial cycles in their southern portion and have been severely disrupted mainly due to recent human activities. Additionally, the landscape is characterized by a series of potential barriers to gene flow, such as the Chacao Channel, Cordillera de Piuche in Chiloé and both the Ancud and the Corcovado gulfs. We used mitochondrial DNA sequences and microsatellite data across several populations to evaluate the genetic variability and structure of the sigmodontine rodent Abrothrix olivacea brachiotis, one of the most common species of small mammals and an inhabitant of these biodiverse forests. Sequencing data showed that along with the recovery of high haplotype variation for this species, there was a low nucleotide diversity between haplotypes, showing no genetic differences between the Chiloé Island and continental populations in southern Chile or through any other geographic barrier in the study area. However, microsatellite data exhibited some level of population structuring. The most evident clusterings were those of the Chiloé Island and that of North Patagonia. These findings are corroborated by a barrier analysis that showed a genetic barrier in the latter areas, whereas the Chacao Channel was not a significant barrier for this rodent. Overall, the genetic variability and structure of A. o. brachiotis was concordant with historical factors, such as the Last Glacial Maximum and the presence of geographic elements that isolate populations.

Interspecific geographic range size-body size relationship and the diversification dynamics of Neotropical furnariid birds.

Among the earliest macroecological patterns documented, is the range and body size relationship, characterized by a minimum geographic range size imposed by the species' body size. This boundary for the geographic range size increases linearly with body size and has been proposed to have implications in lineages evolution and conservation. Nevertheless, the macroevolutionary processes involved in the origin of this boundary and its consequences on lineage diversification have been poorly explored. We evaluate the macroevolutionary consequences of the difference (hereafter the distance) between the observed and the minimum range sizes required by the species' body size, to untangle its role on the diversification of a Neotropical species-rich bird clade using trait-dependent diversification models. We show that speciation rate is a positive hump-shaped function of the distance to the lower boundary. The species with highest and lowest distances to minimum range size had lower speciation rates, while species close to medium distances values had the highest speciation rates. Further, our results suggest that the distance to the minimum range size is a macroevolutionary constraint that affects the diversification process responsible for the origin of this macroecological pattern in a more complex way than previously envisioned.

A new species of Austrocodrus Ogloblin (Hymenoptera, Proctotrupidae, Austroserphinae), a Gondwanic relict from southernmost South America.

Austrocodrusgladiogeminus sp. n. is described from southernmost South America. It is a member of the primitive subfamily Austroserphinae (Hymenoptera, Proctotrupidae), which is distributed in Oceania and South America, and is characterized from other Austrocodrus species by its relatively larger body size, the presence of long and sword-shaped ovipositor sheaths, M arising very close and distal to 1cu-a, and Cu and m-cu joining at a distance equivalent to the length of 2cu-a. We consider this species to be a Gondwanan relict. It has southernmost distribution of any proctotrupid.

Historical dynamics and current environmental effects explain the spatial distribution of species richness patterns of New World monkeys.

BACKGROUND: Why biodiversity is not uniformly distributed on the Earth is a major research question of biogeography. One of the most striking patterns of disparity in species distribution are the biodiversity hotspots, which generally do not fit with the distribution of relevant components of the Neotropical biota. In this study, we assess the proximal causes of the species-richness pattern of one of the most conspicuous groups of Neotropical mammals, the New World monkeys the Platyrrhini. We test two complementary hypotheses: (1) there is a historical source-sink dynamic (addressed using macroevolutionary and macroecological approaches); (2) the large number of species in the Amazon basin is due to the constraints imposed by environmental variables occurring outside this area. METHODS: We first characterize spatial patterns of species richness and biodiversity hotspots using a new, objective protocol based on probabilities. Then we evaluate the source-sink hypothesis using BioGeoBEARS analysis and nestedness analysis of species richness patterns. Complementarily, to measure how often different species pairs appear in the same sites, we used null models to estimate the checkerboard score index (C-score). Finally, we evaluate the relationship between several climatic variables and species richness through ordinary least squares (OLS) and spatial autoregressive (SAR) models, and the potential environmental constraints on the pattern. RESULTS: We found one significant cluster of high values for species richness in the Amazon basin. Most dispersal events occurred from the Amazonian subregion to other Neotropical areas. Temperature (T), discrepancy (BR), and NODF indexes show a significant nesting in the matrix ordered by species richness and available energy. The C-score observed was significantly smaller than the null expectation for all sites in the Neotropics where there are records of platyrrhine species. Ten climatic variables comprised the best-fitting model that explains species richness. OLS and SAR models show that this set of variables explains 69.9% and 64.2% of species richness, respectively. Potential of evapotranspiration is the most important variable within this model, showing a linear positive relationship with species richness, and clear lower and upper limits to the species richness distribution. DISCUSSION: We suggest that New World monkeys historically migrated from their biodiversity hotspot (energetically optimal areas for most platyrrine species) to adjacent, energetically suboptimal areas, and that the different dispersal abilities of these species, the lack of competitive interactions at a macroecological scale, and environmental constraints (i.e., energy availability, seasonality) are key elements which explain the non-uniform pattern of species richness for this clade.

Does silvoagropecuary landscape fragmentation affect the genetic diversity of the sigmodontine rodent Oligoryzomys longicaudatus?

BACKGROUND: Fragmentation of native forests is a highly visible result of human land-use throughout the world. In this study, we evaluated the effects of landscape fragmentation and matrix features on the genetic diversity and structure of Oligoryzomys longicaudatus, the natural reservoir of Hantavirus in southern South America. We focused our work in the Valdivian Rainforest where human activities have produced strong change of natural habitats, with an important number of human cases of Hantavirus. METHODS: We sampled specimens of O. longicaudatus from five native forest patches surrounded by silvoagropecuary matrix from Panguipulli, Los Rios Region, Chile. Using the hypervariable domain I (mtDNA), we characterized the genetic diversity and evaluated the effect of fragmentation and landscape matrix on the genetic structure of O. longicaudatus. For the latter, we used three approaches: (i) Isolation by Distance (IBD) as null model, (ii) Least-cost Path (LCP) where genetic distances between patch pairs increase with cost-weighted distances, and (iii) Isolation by Resistance (IBR) where the resistance distance is the average number of steps that is needed to commute between the patches during a random walk. RESULTS: We found low values of nucleotide diversity (π) for the five patches surveyed, ranging from 0.012 to 0.015, revealing that the 73 sampled specimens of this study belong to two populations but with low values of genetic distance (γST ) ranging from 0.022 to 0.099. Likewise, we found that there are no significant associations between genetic distance and geographic distance for IBD and IBR. However, we found for the LCP approach, a significant positive relationship (r = 0.737, p = 0.05), with shortest least-cost paths traced through native forest and arborescent shrublands. DISCUSSION: In this work we found that, at this reduced geographical scale, Oligoryzomys longicaudatus shows genetic signs of fragmentation. In addition, we found that connectivity between full growth native forest remnants is mediated by the presence of dense shrublands and native forest corridors. In this sense, our results are important because they show how native forest patches and associated routes act as source of vector species in silvoagropecuary landscape, increasing the infection risk on human population. This study is the first approach to understand the epidemiological spatial context of silvoagropecuary risk of Hantavirus emergence. Further studies are needed to elucidate the effects of landscape fragmentation in order to generate new predictive models based on vector intrinsic attributes and landscape features.

Phylogenetic evaluation of taxonomic definition of didelphid mouse opossum of the genus Thylamys from valleys of Coquimbo region, Chile.

Only two species of Didelphidae are currently recognized in Chile, the sister species Thylamys elegans, endemic of Mediterranean ecorregion and Thylamys pallidior, the inhabitant of the Puna and desert canyons. Three subspecies have been described for T. elegans: T. e. elegans, T. e. coquimbensis and T. e. soricinus. However, a recent study based on morphological analyses, synonymized T. elegans coquimbensis from the Coquimbo valleys (30-31° S) with T. pallidior and proposed that T. elegans and T. pallidior could be in sympatry at Coquimbo valleys between Fray Jorge (30°40'S) and Paiguano (30°02' S). We assess the current definition of T. e. coquimbensis and T. e. elegans, as well as this taxonomical conflict among the mouse opossums from the Coquimbo valleys through phylogenetic analyses of cytochrome b mitochondrial gene sequences. In this study, for the first time, we used specimens from the type localities of T. e. coquimbensis and T. e. elegans. In addition, we analyzed diagnostic cranial structures for this taxonomic revision. The results supported two allopatric clades, allowing us to keep the taxonomic definition of T. e. elegans and T. e. coquimbensis as phylogenetic reciprocal monophyletic clades and polyphyletic with T. pallidior. This result corroborates previous morphological analyses, which support that mouse opossums from the Coquimbo valleys are T. e. coquimbensis, thus extending its geographic distribution to the coast of Coquimbo and Atacama regions. We don´t have evidence for sympatric distribution between T. elegans and T. pallidior in the Coquimbo region.

Correlated evolution between mode of larval development and habitat in muricid gastropods.

Larval modes of development affect evolutionary processes and influence the distribution of marine invertebrates in the ocean. The decrease in pelagic development toward higher latitudes is one of the patterns of distribution most frequently discussed in marine organisms (Thorson's rule), which has been related to increased larval mortality associated with long pelagic durations in colder waters. However, the type of substrate occupied by adults has been suggested to influence the generality of the latitudinal patterns in larval development. To help understand how the environment affects the evolution of larval types we evaluated the association between larval development and habitat using gastropods of the Muricidae family as a model group. To achieve this goal, we collected information on latitudinal distribution, sea water temperature, larval development and type of substrate occupied by adults. We constructed a molecular phylogeny for 45 species of muricids to estimate the ancestral character states and to assess the relationship between traits using comparative methods in a Bayesian framework. Our results showed high probability for a common ancestor of the muricids with nonpelagic (and nonfeeding) development, that lived in hard bottoms and cold temperatures. From this ancestor, a pelagic feeding larva evolved three times, and some species shifted to warmer temperatures or sand bottoms. The evolution of larval development was not independent of habitat; the most probable evolutionary route reconstructed in the analysis of correlated evolution showed that type of larval development may change in soft bottoms but in hard bottoms this change is highly unlikely. Lower sea water temperatures were associated with nonpelagic modes of development, supporting Thorson's rule. We show how environmental pressures can favor a particular mode of larval development or transitions between larval modes and discuss the reacquisition of feeding larva in muricids gastropods.

Colony size evolution and the origin of eusociality in corbiculate bees (Hymenoptera: Apinae).

Recently, it has been proposed that the one of the main determinants of complex societies in Hymenoptera is colony size, since the existence of large colonies reduces the direct reproductive success of an average individual, given a decreased chance of being part of the reproductive caste. In this study, we evaluate colony size evolution in corbiculate bees and their relationship with the sociality level shown by these bees. Specifically i) the correlation between colony size and level of sociality considering the phylogenetic relationship to evaluate a general evolutionary tendency, and ii) the hypothetical ancestral forms of several clades within a phylogeny of corbiculate bees, to address idiosyncratic process occurring at important nodes. We found that the level of social complexity in corbiculate bees is phylogenetically correlated with colony size. Additionally, another process is invoked to propose why colony size evolved concurrently with the level of social complexity. The study of this trait improves the understanding of the evolutionary transition from simple to complex societies, and highlights the importance of explicit probabilistic models to test the evolution of other important characters involved in the origin of eusociality.

Body size evolution in extant Oryzomyini rodents: Cope's rule or miniaturization?

At the macroevolutionary level, one of the first and most important hypotheses that proposes an evolutionary tendency in the evolution of body sizes is "Cope's rule". This rule has considerable empirical support in the fossil record and predicts that the size of species within a lineage increases over evolutionary time. Nevertheless, there is also a large amount of evidence indicating the opposite pattern of miniaturization over evolutionary time. A recent analysis using a single phylogenetic tree approach and a bayesian based model of evolution found no evidence for Cope's rule in extant mammal species. Here we utilize a likelihood-based phylogenetic method, to test the evolutionary trend in body size, which considers phylogenetic uncertainty, to discern between Cope's rule and miniaturization, using extant Oryzomyini rodents as a study model. We evaluated body size trends using two principal predictions: (a) phylogenetically related species are more similar in their body size, than expected by chance; (b) body size increased (Cope's rule)/decreased (miniaturization) over time. Consequently the distribution of forces and/or constraints that affect the tendency are homogenous and generate this directional process from a small/large sized ancestor. Results showed that body size in the Oryzomyini tribe evolved according to phylogenetic relationships, with a positive trend, from a small sized ancestor. Our results support that the high diversity and specialization currently observed in the Oryzomyini tribe is a consequence of the evolutionary trend of increased body size, following and supporting Cope's rule.

The evolution of ecomorphological traits within the Abrothrichini (Rodentia: Sigmodontinae): a Bayesian phylogenetics approach.

The generally accepted hypothesis regarding the origin of fossorial mammals proposes adaptive convergence from open environments towards the use of subterranean environments. We evaluated this hypothesis for South American mole-mice using conventional and Bayesian frameworks, with independent evidence. By using a molecular approach based on Cytochrome b and IRBP sequences, we evaluated phylogenetic relationships, time of origin, the ancestral trait of fossoriality, and ancestral distributions of species belonging to the Andean Clade (Rodentia: Sigmodontinae). Our results indicate that the Andean Clade is highly sustained; with one clade grouping all fossorial forms and another grouping all cursorial species. We hypothesized that fossoriality originated in the Miocene/Pliocene transition, in the Temperate Forests of southern South America. We conclude that the origin of fossorial ecomorphological traits did not necessarily occur under a general model of open environments, the origin of these traits depends on the ecological-historical relationship of the taxon with the environment.