How Important Is Budding Speciation for Comparative Studies?

The acknowledgment of evolutionary dependence among species has fundamentally changed how we ask biological questions. Phylogenetic models became the standard approach for studies with 3 or more lineages, in particular those using extant species. Most phylogenetic comparative methods (PCMs) translate relatedness into covariance, meaning that evolutionary changes before lineages split should be interpreted together whereas after the split lineages are expected to change independently. This clever realization has shaped decades of research. Here, we discuss one element of the comparative method often ignored or assumed as unimportant: if nodes of a phylogeny represent the dissolution of the ancestral lineage into two new ones or if the ancestral lineage can survive speciation events (i.e., budding). Budding speciation is often reported in paleontological studies, due to the nature of the evidence for budding in the fossil record, but it is surprisingly absent in comparative methods. Here, we show that many PCMs assume that divergence happens as a symmetric split, even if these methods do not explicitly mention this assumption. We discuss the properties of trait evolution models for continuous and discrete traits and their adequacy under a scenario of budding speciation. We discuss the effects of budding speciation under a series of plausible evolutionary scenarios and show when and how these can influence our estimates. We also propose that long-lived lineages that have survived through a series of budding speciation events and given birth to multiple new lineages can produce evolutionary patterns that challenge our intuition about the most parsimonious history of trait changes in a clade. We hope our discussion can help bridge comparative approaches in paleontology and neontology as well as foster awareness about the assumptions we make when we use phylogenetic trees.

Reconstructing Squamate Biogeography in Afro-Arabia Reveals the Influence of a Complex and Dynamic Geologic Past.

The geographic distribution of biodiversity is central to understanding evolutionary biology. Paleogeographic and paleoclimatic histories often help to explain how biogeographic patterns unfold through time. However, such patterns are also influenced by a variety of other factors, such as lineage diversification, that may affect the probability of certain types of biogeographic events. The complex and well-known geologic and climatic history of Afro-Arabia, together with the extensive research on reptile systematics in the region, makes Afro-Arabian squamate communities an ideal system to investigate biogeographic patterns and their drivers. Here, we reconstruct the phylogenetic relationships and the ancestral geographic distributions of several Afro-Arabian reptile clades (totaling 430 species) to estimate the number of dispersal, vicariance and range contraction events. We then compare the observed biogeographic history to a distribution of simulated biogeographic events based on the empirical phylogeny and the best-fit model. This allows us to identify periods in the past where the observed biogeographic history was likely shaped by forces beyond the ones included in the model. We find an increase in vicariance following the Oligocene, most likely caused by the fragmentation of the Afro-Arabian plate. In contrast, we did not find differences between observed and expected dispersal and range contraction levels. This is consistent with diversification enhanced by environmental processes and with the establishment of a dispersal corridor connecting Africa, Arabia and Eurasia since the middle Miocene. Finally, here we show that our novel approach is useful to pinpoint events in the evolutionary history of lineages that might reflect external forces not predicted by the underlying biogeographic model. [Dispersal; diversification; model adequacy; paleogeography; reptiles; simulations; vicariance.].

Comparative Analyses of Phenotypic Sequences Using Phylogenetic Trees.

Phenotypic sequences are a type of multivariate trait organized structurally, such as teeth distributed along the dental arch, or temporally, such as the stages of an ontogenetic series. Unlike other multivariate traits, the elements of a phenotypic sequence are distributed along an ordered set, which allows for distinct evolutionary patterns between neighboring and distant positions. In fact, sequence traits share many characteristics with molecular sequences, although important distinctions pose challenges to current comparative methods. We implement an approach to estimate rates of trait evolution that explicitly incorporates the sequence organization of traits. We apply models to study the temporal pattern evolution of cricket calling songs. We test whether neighboring positions along a phenotypic sequence have correlated rates of evolution or whether rate variation is independent of sequence position. Our results show that cricket song evolution is strongly autocorrelated and that models perform well when used with sequence phenotypes even under small sample sizes. Our approach is flexible and can be applied to any multivariate trait with discrete units organized in a sequence-like structure.

Comparative Analysis of Principal Components Can be Misleading.

Most existing methods for modeling trait evolution are univariate, although researchers are often interested in investigating evolutionary patterns and processes across multiple traits. Principal components analysis (PCA) is commonly used to reduce the dimensionality of multivariate data so that univariate trait models can be fit to individual principal components. The problem with using standard PCA on phylogenetically structured data has been previously pointed out yet it continues to be widely used in the literature. Here we demonstrate precisely how using standard PCA can mislead inferences: The first few principal components of traits evolved under constant-rate multivariate Brownian motion will appear to have evolved via an "early burst" process. A phylogenetic PCA (pPCA) has been proprosed to alleviate these issues. However, when the true model of trait evolution deviates from the model assumed in the calculation of the pPCA axes, we find that the use of pPCA suffers from similar artifacts as standard PCA. We show that data sets with high effective dimensionality are particularly likely to lead to erroneous inferences. Ultimately, all of the problems we report stem from the same underlying issue--by considering only the first few principal components as univariate traits, we are effectively examining a biased sample of a multivariate pattern. These results highlight the need for truly multivariate phylogenetic comparative methods. As these methods are still being developed, we discuss potential alternative strategies for using and interpreting models fit to univariate axes of multivariate data.

The ecological tale of Gonyleptidae (Arachnida, Opiliones) evolution: phylogeny of a Neotropical lineage of armoured harvestmen using ecological, behavioural and chemical characters.

The large Neotropical family Gonyleptidae comprises nearly 820 species divided into 16 subfamilies. The majority of publications on harvestman ecology, behaviour and scent gland secretion chemistry have focused on this family. We used the information available in the literature and combined it with an intensive search for ecological, behavioural and chemical data to infer the phylogeny of the Gonyleptidae. We included 28 species belonging to 14 of the 16 gonyleptid subfamilies in the ingroup and four species belonging to the families Cosmetidae, Stygnidae and Manaosbiidae in the outgroup. We performed the analyses using equally weighted characters and coded 63 characters comprising 153 states, which makes this the largest non-morphological, non-molecular phylogenetic data matrix published to date. We obtained five most parsimonious trees, and the strict consensus resulted in six collapsed nodes. The results show that the monophyly of Gonyleptidae is equivocal because Metasarcinae is placed at a basal polytomy with the outgroups Cosmetidae and Stygnidae. Gonyleptinae, Pachylinae and Progonyleptoidellinae are polyphyletic groups, but the remaining subfamilies are monophyletic and have several synapomorphies. Based on the resulting topology, we discuss the performance of ecological, behavioural and chemical characters, and map a selected set of characters to discuss their evolutionary patterns in the family.

Copelatus cessaima sp. nov. (Coleoptera: Dytiscidae: Copelatinae): first record of a troglomorphic diving beetle from Brazil.

Copelatus cessaima sp. nov. is described from Brazil. The new species was collected in water puddles inside of caves found in an ironstone formation and has typical troglomorphic characters: the eyes and metathoracic wings are absent, the elytra are fused and the body has long setae. This is the second species of Copelatinae reported as troglomorphic and the first record of a troglomorphic Dytiscidae species in Brazil. The modified morphology of the new species and the lack of elytral striae make the placement of C. cessaima sp. nov. in one of the 15 recognized Copelatus species groups difficult. Thus, we assign the new species to a "group unknown" as defined in Nilsson's world catalogue of the family Dytiscidae.

Hidden state models improve state-dependent diversification approaches, including biogeographical models.

The state-dependent speciation and extinction (SSE) models have recently been criticized due to their high rates of "false positive" results. Many researchers have advocated avoiding SSE models in favor of other "nonparametric" or "semiparametric" approaches. The hidden Markov modeling (HMM) approach provides a partial solution to the issues of model adequacy detected with SSE models. The inclusion of "hidden states" can account for rate heterogeneity observed in empirical phylogenies and allows for reliable detection of state-dependent diversification or diversification shifts independent of the trait of interest. However, the adoption of HMM has been hampered by the interpretational challenges of what exactly a "hidden state" represents, which we clarify herein. We show that HMMs in combination with a model-averaging approach naturally account for hidden traits when examining the meaningful impact of a suspected "driver" of diversification. We also extend the HMM to the geographic state-dependent speciation and extinction (GeoSSE) model. We test the efficacy of our "GeoHiSSE" extension with both simulations and an empirical dataset. On the whole, we show that hidden states are a general framework that can distinguish heterogeneous effects of diversification attributed to a focal character.

A new species of the genus Pimelerodius Vanin from the Amazon Region, with notes on the geografic distribution of Pimelerodius motacilla (Boheman) (Coleoptera, Curculionidae, Otidocephalini) / Nova espécie do gênero Pimelerodius Vanin da Região Amazônica, com comentários sobre a distribuição geográfica de Pimelerodius motacilla (Boheman) (Coleoptera, Curculionidae, Otidocephalini)

Pimelerodius punctiventris sp. nov. (type locality Brazil, Amazonas, Itacoatiara) is described and illustrated. The new taxon is compared with similar species, being distinguished from the other 12 known species of the genus by the presence of punctures in ventrite I. The available published key for identification of species of Pimelerodius is adapted to include the new species. A modification of the generic description of the aedeagus of Pimelerodius is provided, a necessity due to the differences observed in the aedeagus of the new species. The occurrence of P. motacilla (Boheman, 1843) in the Amazon Region, recorded in sympatry with P. punctiventris in Itacoatiara, AM, is discussed and confirmed, based on the study of 41 available specimens.

Pimelerodius punctiventris sp. nov. (localidade-tipo, Brasil, Amazonas, Itacoatiara) é descrita e ilustrada. O táxon novo é comparado com espécies semelhantes, diferindo das outras 12 espécies conhecidas do gênero pela presença de pontuações no ventrito I. A chave disponível para a identificação das espécies de Pimelerodius é adaptada para incluir a nova espécie. A descrição do edeago do gênero Pimelerodius precisou ser alterada, conseqüência das diferenças observadas no edeago da nova espécie. A ocorrência de P. motacilla (Boheman, 1843) na Região Amazônica, registrada em simpatria com P. punctiventris em Itacoatiara, AM, é discutida e confirmada, com base em 41 exemplares examinados.