Faster evolution of a premating reproductive barrier is not associated with faster speciation rates in New World passerine birds

Why are speciation rates so variable across the tree of life? One hypothesis is that this variation is explained by how rapidly reproductive barriers evolve. We tested this hypothesis by conducting a comparative study of the evolution of bird song, a premating barrier to reproduction. Speciation in birds is typically initiated when geographically isolated (allopatric) populations evolve reproductive barriers. We measured the strength of song as a premating barrier between closely related allopatric populations by conducting 2339 field experiments to measure song discrimination for 175 taxon pairs of allopatric or parapatric New World passerine birds, and estimated recent speciation rates from molecular phylogenies. We found evidence that song discrimination is indeed an important reproductive barrier: taxon pairs with high song discrimination in allopatry did not regularly interbreed in parapatry. However, evolutionary rates of song discrimination were not associated with recent speciation rates. Evolutionary rates of song discrimination were also unrelated to latitude or elevation, but species with innate song (suboscines) evolved song discrimination much faster than species with learned song (oscines). We conclude that song is a key premating reproductive barrier in birds, but faster evolution of this reproductive barrier between populations does not consistently result in faster diversification between species.

A simple island biodiversity model is robust to trait dependence in diversification and colonization rates

The application of state-dependent speciation and extinction (SSE) models to phylogenetic trees has revealed an important role for traits in diversification. However, this role remains comparatively unexplored on islands, which can include multiple independent clades resulting from different colonization events. Here, we perform a robustness study to identify how trait-dependence in rates of island colonization, extinction and speciation (CES rates) affects the estimation accuracy of a phylogenetic model that assumes no rate variation between trait states. We extend the DAISIE (Dynamic Assembly of Islands through Speciation, Immigration and Extinction) simulation model to include state-dependent rates, and evaluate the robustness of the DAISIE inference model using simulated data. Our results show that when the CES rate differences between trait states are moderate, DAISIE shows negligible error for a variety of island diversity metrics. However, for large differences in speciation rates, we find large errors when reconstructing clade size variation and non-endemic species diversity through time. We conclude that for many biologically realistic scenarios with trait-dependent speciation and colonization, island diversity dynamics can be accurately estimated without the need to explicitly model trait dynamics. Nonetheless, our new simulation model may provide a useful tool for studying patterns of trait variation.

Macroevolutionary consequences of mast seeding

Masting characterizes large, intermittent and highly synchronous seeding events among individual plants and is found throughout the plant Tree of Life (ToL). Although masting can increase plant fitness, little is known about whether it results in evolutionary changes across entire clades, such as by promoting speciation or enhanced trait selection. Here, we tested if masting has macroevolutionary consequences by combining the largest existing dataset of population-level reproductive time series and time-calibrated phylogenetic tree of vascular plants. We found that the coefficient of variation (CV p ) of reproductive output for 307 species covaried with evolutionary history, and more so within clades than expected by random. Speciation rates estimated at the species level were highest at intermediate values of CV p and regional-scale synchrony (S r ) in seed production, that is, there were unimodal correlations. There was no support for monotonic correlations between either CV p or S r and rates of speciation or seed size evolution. These results were robust to different sampling decisions, and we found little bias in our dataset compared with the wider plant ToL. While masting is often adaptive and encompasses a rich diversity of reproductive behaviours, we suggest it may have few consequences beyond the species level. This article is part of the theme issue ‘The ecology and evolution of synchronized seed production in plants’.

Earth history events shaped the evolution of uneven biodiversity across tropical moist forests

Far from a uniform band, the biodiversity found across Earth’s tropical moist forests varies widely between the high diversity of the Neotropics and Indomalaya and the relatively lower diversity of the Afrotropics. Explanations for this variation across different regions, the “pantropical diversity disparity” (PDD), remain contentious, due to difficulty teasing apart the effects of contemporary climate and paleoenvironmental history. Here, we assess the ubiquity of the PDD in over 150,000 species of terrestrial plants and vertebrates and investigate the relationship between the present-day climate and patterns of species richness. We then investigate the consequences of paleoenvironmental dynamics on the emergence of biodiversity gradients using a spatially explicit model of diversification coupled with paleoenvironmental and plate tectonic reconstructions. Contemporary climate is insufficient in explaining the PDD; instead, a simple model of diversification and temperature niche evolution coupled with paleoaridity constraints is successful in reproducing the variation in species richness and phylogenetic diversity seen repeatedly among plant and animal taxa, suggesting a prevalent role of paleoenvironmental dynamics in combination with niche conservatism. The model indicates that high biodiversity in Neotropical and Indomalayan moist forests is driven by complex macroevolutionary dynamics associated with mountain uplift. In contrast, lower diversity in Afrotropical forests is associated with lower speciation rates and higher extinction rates driven by sustained aridification over the Cenozoic. Our analyses provide a mechanistic understanding of the emergence of uneven diversity in tropical moist forests across 110 Ma of Earth’s history, highlighting the importance of deep-time paleoenvironmental legacies in determining biodiversity patterns.

Conserved ancestral tropical niche but different continental histories explain the latitudinal diversity gradient in brush-footed butterflies

The global increase in species richness toward the tropics across continents and taxonomic groups, referred to as the latitudinal diversity gradient, stimulated the formulation of many hypotheses to explain the underlying mechanisms of this pattern. We evaluate several of these hypotheses to explain spatial diversity patterns in a butterfly family, the Nymphalidae, by assessing the contributions of speciation, extinction, and dispersal, and also the extent to which these processes differ among regions at the same latitude. We generate a time-calibrated phylogeny containing 2,866 nymphalid species (~45% of extant diversity). Neither speciation nor extinction rate variations consistently explain the latitudinal diversity gradient among regions because temporal diversification dynamics differ greatly across longitude. The Neotropical diversity results from low extinction rates, not high speciation rates, and biotic interchanges with other regions are rare. Southeast Asia is also characterized by a low speciation rate but, unlike the Neotropics, is the main source of dispersal events through time. Our results suggest that global climate change throughout the Cenozoic, combined with tropical niche conservatism, played a major role in generating the modern latitudinal diversity gradient of nymphalid butterflies.

Evolution of degrees of carnivory and dietary specialization across Mammalia and their effects on speciation

ABSTRACTConflation between omnivory and dietary generalism limits ecological and evolutionary analyses of diet, including estimating contributions to speciation and diversification. Additionally, categorizing species into qualitative dietary classes leads to information loss in these analyses. Here, we constructed two continuous variables – degree of carnivory (i.e., the position along the continuum from complete herbivory to complete carnivory) and degree of dietary specialization (i.e., the number and variety of food resources utilized) – to elucidate their histories across Mammalia, and to tease out their independent contributions to mammalian speciation. We observed that degree of carnivory significantly affected speciation rate across Mammalia, whereas dietary specialization did not. We further considered phylogenetic scale in diet-dependent speciation and saw that degree of carnivory significantly affected speciation in ungulates, carnivorans, bats, eulipotyphlans, and marsupials, while the effect of dietary specialization was only significant in carnivorans. Across Mammalia, omnivores had the lowest speciation rates. Our analyses using two different categorical diet variables led to contrasting signals of diet-dependent diversification, and subsequently different conclusions regarding diet’s macroevolutionary role. We argue that treating variables such as diet as continuous instead of categorical reduces information loss and avoids the problem of contrasting macroevolutionary signals caused by differential discretization of biologically continuous traits.

Niche shifts after island colonization spurred adaptive diversification and speciation in a cosmopolitan bird clade

Islands have long been recognized as key contributors to biodiversity because they facilitate geographic isolation and ecological divergence from mainland ancestors. However, island colonization has traditionally been considered an evolutionary dead-end process, and its consequences for continental biodiversity remain understudied. Here, we use the evolutionary radiation of Columbiformes (i.e. pigeons and doves) to examine if ecological niche shifts on islands shaped biological diversification and community composition on continents. We show that the colonization of islands by continental, terrestrial-foraging lineages led to the exploitation of a new ecological niche (i.e. arboreal foraging). This transition towards arboreal foraging was associated with evolutionary adaptation towards a new morphological optimum. In addition, arboreal-foraging lineages of islands experienced an increase in speciation rates, which was associated with successful range expansions to other islands as well as back colonization of continents. Our results provide empirical evidence that diversification on continents can only be fully understood when studying the diversification processes that took place on islands, challenging the view of islands as mere sinks of evolutionary diversity.

An early burst in brachiopod evolution corresponding with significant climatic shifts during the Great Ordovician Biodiversification Event

We employ modified tip-dating methods to date divergence times within the Strophomenoidea, one of the most abundant and species-rich brachiopod clades to radiate during the Great Ordovician Biodiversification Event (GOBE), to determine if significant environmental changes at this time correlate with the diversification of the clade. Models using origination, extinction and sampling rates to estimate prior probabilities of divergence times strongly support both high rates of anatomical change per million years and rapid divergences shortly before the clade first appears in the fossil record. These divergence times indicate much higher rates of cladogenesis than are typical of brachiopods during this interval. The correspondence of high speciation rates and high anatomical disparity suggests punctuated (speciational) change drove the high frequencies of early anatomical change, which in turn suggests increased ecological opportunities rather than shifting developmental constraints account for high rates of anatomical change. The pulse of rapid evolution began coincident with cooling temperatures, the start of major oscillations in sea level and increased levels of atmospheric oxygen. Our results suggest that these factors permitted major geographical and ecological expansion of strophomenoids with intervals of geographical isolation, resulting in elevated speciation rates and corresponding elevated frequencies of punctuated change.

Investigating the reliability of molecular estimates of evolutionary time when substitution rates and speciation rates vary

Background An accurate timescale of evolutionary history is essential to testing hypotheses about the influence of historical events and processes, and the timescale for evolution is increasingly derived from analysis of DNA sequences. But variation in the rate of molecular evolution complicates the inference of time from DNA. Evidence is growing for numerous factors, such as life history and habitat, that are linked both to the molecular processes of mutation and fixation and to rates of macroevolutionary diversification. However, the most widely used models of molecular rate variation, such as the uncorrelated and autocorrelated lognormal clocks, rely on idealised models of rate variation and molecular dating methods are rarely tested against complex models of rate change. One relationship that is not accounted for in molecular dating is the potential for interaction between molecular substitution rates and speciation, a relationship that has been supported by empirical studies in a growing number of taxa. If these relationships are as widespread as evidence indicates, they may have a significant influence on molecular dates. Results We simulate phylogenies and molecular sequences under three different realistic rate variation models - one in which speciation rates and substitution rates both vary but are unlinked, one in which they covary continuously and one punctuated model in which molecular change is concentrated in speciation events, using empirical case studies to parameterise realistic simulations. We test two commonly used "relaxed clock" molecular dating methods against these realistic simulations to explore the degree of error in molecular dates under each model. We find average divergence time inference errors ranging from 12% of node age for the unlinked model when reconstructed under an uncorrelated rate prior, to up to 93% when punctuated simulations are reconstructed under an autocorrelated prior. Conclusions We demonstrate the potential for substantial errors in molecular dates when both speciation rates and substitution rates vary between lineages. This study highlights the need for tests of molecular dating methods against realistic models of rate variation generated from empirical parameters and known relationships.