Papers by Felipe Bandoni de Oliveira
The sudden appearance of platyrrhine primates and caviomorph rodents in the late Oligocene fossil... more The sudden appearance of platyrrhine primates and caviomorph rodents in the late Oligocene fossil record comprises an old puzzle for biologists and paleontologists, since South America was an isolated continent for most of the Tertiary. The well-established phylogenetic relationships between these groups and African forms force acceptance of some kind of migration across the Atlantic Ocean. Many hypotheses have been put forward to account for this crossing, including floating island rafting, volcanic stepping-stone islands, and land bridges. Here we present paleogeographic reconstructions of the South Atlantic in order to re-evaluate the scenario in which such migration took place, modeling both continental drift and sea-floor thermal subsidence movements, while accounting for sea level changes. We analyse these data by bringing together evidence from the fossil record, estimated dates of phylogenetic divergence based on molecular data, geophysical modeling and paleocurrent estimates. Our reconstructions confirmed previous findings that reject complete land bridges between Africa and South America during the Cenozoic, but suggested the presence of islands of considerable size (>200 km in length) in the South Atlantic. Other paleogeographic features that could eventually reduce migration distance are discussed. Our data indicated that the most favorable period for a possible Africa--South America migration was between 40 and 50 million years ago. This evidence, coupled with favorable westward paleocurrents and paleowinds from Africa could have facilitated a transatlantic crossing via floating islands. Other organisms that seem to share the distributional patterns of platyrrhines and caviomorphs could also have dispersed between Africa and South America in this scenario.
The study of the genetic variance/covariance matrix (G-matrix) is a recent and fruitful approach ... more The study of the genetic variance/covariance matrix (G-matrix) is a recent and fruitful approach in evolutionary biology, providing a window to investigate the evolution of complex characters. Although G-matrix studies were originally conducted for microevolutionary timescales, they could be extrapolated to macroevolution as long as the G-matrix remains relatively constant, or proportional, along the period of interest. A promising approach to investigate the constancy of G-matrices is to compare their phenotypic counterparts (P-matrices) in a large group of related species; if significant similarity is found among several taxa, it is very likely that the underlying G-matrices are also equivalent. Here we studied the similarity of covariance and correlation structure in a broad sample of Old World monkeys and apes (Catarrhini). We made phylogenetically structured comparisons of correlation and covariance matrices derived from 39 skull traits, ranging from between species to the superfamily level. We also compared the overall magnitude of integration between skull traits (r2) for all Catarrhini genera. Our results showed that P-matrices were not strictly constant among catarrhines, but the amount of divergence observed among taxa was generally low. There was significant and positive correlation between the amount of divergence in correlation and covariance patterns among the 30 genera and their phylogenetic distance derived from a recently proposed phylogenetic hypothesis. Our data demonstrate that the P-matrices were kept relatively similar along the evolutionary history of catarrhines, and comparisons with the G-matrix available for a New World monkey genus (Saguinus) suggests that the same holds for all anthropoids. The magnitude of integration, in contrast, presented considerable variation between genera, indicating that evolution of the magnitude, rather than the pattern of inter-trait correlations, might have played an important role on the diversification of the catarrhine skull.
Allometry is a major determinant of within-population patterns of association among traits and, t... more Allometry is a major determinant of within-population patterns of association among traits and, therefore, a major component of morphological integration studies. Even so, the influence of size variation over evolutionary change has been largely unappreciated. Here, we explore the interplay between allometric size variation, modularity, and life-history strategies in the skull from representatives of 35 mammalian families. We start by removing size variation from within-species data and analyzing its influence on integration magnitudes, modularity patterns, and responses to selection. We also carry out a simulation in which we artificially alter the influence of size variation in within-taxa matrices. Finally, we explore the relationship between size variation and different growth strategies. We demonstrate that a large portion of the evolution of modularity in the mammalian skull is associated to the evolution of growth strategies. Lineages with highly altricial neonates have adult variation patterns dominated by size variation, leading to high correlations among traits regardless of any underlying modular process and impacting directly their potential to respond to selection. Greater influence of size variation is associated to larger intermodule correlations, less individualized modules, and less flexible responses to natural selection.
Changes in patterns and magnitudes of integration may influence the ability of a species to respo... more Changes in patterns and magnitudes of integration may influence the ability of a species to respond to selection. Consequently, modularity has often been linked to the concept of evolvability, but their relationship has rarely been tested empirically. One possible explanation is the lack of analytical tools to compare patterns and magnitudes of integration among diverse groups that explicitly relate these aspects to the quantitative genetics framework. We apply such framework here using the multivariate response to selection equation to simulate the evolutionary behavior of several mammalian orders in terms of their flexibility, evolvability and constraints in the skull. We interpreted these simulation results in light of the integration patterns and magnitudes of the same mammalian groups, described in a companion paper. We found that larger magnitudes of integration were associated with a blur of the modules in the skull and to larger portions of the total variation explained by size variation, which in turn can exert a strong evolutionary constraint, thus decreasing the evolutionary flexibility. Conversely, lower overall magnitudes of integration were associated with distinct modules in the skull, to smaller fraction of the total variation associated with size and, consequently, to weaker constraints and more evolutionary flexibility. Flexibility and constraints are, therefore, two sides of the same coin and we found them to be quite variable among mammals. Neither the overall magnitude of morphological integration, the modularity itself, nor its consequences in terms of constraints and flexibility, were associated with absolute size of the organisms, but were strongly associated with the proportion of the total variation in skull morphology captured by size. Therefore, the history of the mammalian skull is marked by a trade-off between modularity and evolvability. Our data provide evidence that, despite the stasis in integration patterns, the plasticity in the magnitude of integration in the skull had important consequences in terms of evolutionary flexibility of the mammalian lineages.
Morphological integration refers to the modular structuring of inter-trait relationships in an or... more Morphological integration refers to the modular structuring of inter-trait relationships in an organism, which could bias the direction and rate of morphological change, either constraining or facilitating evolution along certain dimensions of the morphospace. Therefore, the description of patterns and magnitudes of morphological integration and the analysis of their evolutionary consequences are central to understand the evolution of complex traits. Here we analyze morphological integration in the skull of several mammalian orders, addressing the following questions: are there common patterns of inter-trait relationships? Are these patterns compatible with hypotheses based on shared development and function? Do morphological integration patterns and magnitudes vary in the same way across groups? We digitized more than 3,500 specimens spanning 15 mammalian orders, estimated the correspondent pooled within-group correlation and variance/covariance matrices for 35 skull traits and compared those matrices among the orders. We also compared observed patterns of integration to theoretical expectations based on common development and function. Our results point to a largely shared pattern of inter-trait correlations, implying that mammalian skull diversity has been produced upon a common covariance structure that remained similar for at least 65 million years. Comparisons with a rodent genetic variance/covariance matrix suggest that this broad similarity extends also to the genetic factors underlying phenotypic variation. In contrast to the relative constancy of inter-trait correlation/covariance patterns, magnitudes varied markedly across groups. Several morphological modules hypothesized from shared development and function were detected in the mammalian taxa studied. Our data provide evidence that mammalian skull evolution can be viewed as a history of inter-module parcellation, with the modules themselves being more clearly marked in those lineages with lower overall magnitude of integration. The implication of these findings is that the main evolutionary trend in the mammalian skull was one of decreasing the constraints to evolution by promoting a more modular architecture.
An interesting case of reproductive specialization among anurans is found in bromeligen species, ... more An interesting case of reproductive specialization among anurans is found in bromeligen species, which have reproductive cycles associated with bromeliads. In these species, male reproductive activity might be related not only to macroclimatic patterns but also to the availability of suitable microhabitats in bromeliads. This research focuses on one bromeligen species from Southeastern Brazil, Scinax perpusillus, which is territorial and uses bromeliads as retreat and oviposition sites. Two populations were studied (Intervales State Park and Boracéia Biological Station, both in the state of São Paulo, Brazil). Available bromeliads vary substantially in morphology and position in the forest, so we ask whether male frogs 1) select plants with specific eco-morphological traits, 2) call at specific time periods within the reproductive season, and 3) call more actively under certain temperature and humidity conditions. The patterns of male calling activity within the reproductive season varied between years and between populations, but calling was not more intense during warmer or more humid periods. It seems, then, that subtle patterns of phenology might vary significant between populations and across years. Bromeliad choice was non-random. Males chose bromeliads that were larger, clustered, closer to the ground, and had higher reservoir pH; features that probably reflect the quality of the plants as oviposition sites, and that might confer social advantages by reducing conflict with neighboring males.
Phenotypic integration is essential to the understanding of organismal evolution as a whole. In t... more Phenotypic integration is essential to the understanding of organismal evolution as a whole. In this study, a phylogenetic framework is used to assess phenotypic integration among the floral parts of a group of Neotropical lianas. Flowers consist of plant reproductive organs (carpels and stamens), usually surrounded by attractive whorls (petals and sepals). Thus, flower parts might be involved in different functions and developmental constraints, leading to conflicting selective forces. We found that Bignonieae flowers have very similar patterns of variance/covariance among traits and that such patterns are uncorrelated with the phylogenetic relationships between species. However, in spite of pattern stasis, our results also indicate that diversification of floral morphology in this group has occurred throughout the evolution of magnitudes of correlation among traits. Thus, we suggest that stabilizing selection has played an important role in phenotypic integration, resulting in the long-term stasis of covariance patterns underlying flower diversification during the ca. 50 Myr of evolution of Bignonieae. This is the first report of long-term stasis in the phenotypic integration of angiosperms, suggesting that patterns of floral morphology can be recognizable as specific attributes of distinct botanical families.
Ectotherm locomotion is restricted by low temperatures and many species, such as some flying inse... more Ectotherm locomotion is restricted by low temperatures and many species, such as some flying insects, need to achieve thermal thresholds before taking off. Body size influences heat exchange between an animal and the environment; therefore, larger animals have higher thermal inertia, and necessarily spend more time warming up before flight, a critical period when they remain exposed and more susceptible to predators. Thus, one could expect larger animals, along their evolutionary history, to have developed a more diversified repertoire of defensive behaviors when compared to smaller counterparts. Moths are an interesting model for testing this hypothesis, as they exhibit considerable variation in body size and many species perform pre-flight warming up by muscle shivering, an evidence of thermal restriction on locomotion. I registered the responses of 76 moths immediately after disturbance, simulating the attack of a predator, and the behavioral response was then associated to body size. I conducted the experiments at 20°C and 25ºC to account for eventual thermal restrictions on behavior, and identified animals to the family level to account for the effect of a common phylogenetic history. When disturbed at 25ºC, smaller moths tend to fly, while the larger tend to run. At 20ºC almost all moths ran, including the smaller animals, an evidence of a possible thermal restriction on flight. There is a more diversified repertoire of defensive behaviors among larger moths, corroborating the proposed hypothesis. An alternative interpretation would be that common behaviors among related moths could be explained by common phylogenetic histories. However, two evidences support the physiological restriction hypothesis: 1) the analysis within Sphingidae and Geometridae (not closely related families) showed similar results to the overall analysis, and 2) a more diverse repertoire of defensive behaviors was associated to a lower, and therefore more restrictive to locomotion, experimental temperature (20°C).
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Papers by Felipe Bandoni de Oliveira