Publications

Summary Powered flight was fundamental to the establishment and radiation of birds. However, flight has been lost multiple times throughout avian evolution. Convergent losses of flight within the ratites (flightless paleognaths, including the emu and ostrich) often coincide with reduced wings. Although there is a wealth of anatomical knowledge for several ratites, the genetic mechanisms causing these changes remain debated. Here, we use a multidisciplinary approach employing embryological, genetic, and genomic techniques to interrogate the mechanisms underlying forelimb heterochrony in emu embryos. We show that the initiation of limb formation, an epithelial to mesenchymal transition (EMT) in the lateral plate mesoderm (LPM) and myoblast migration into the LPM, occur at equivalent stages in the emu and chick. However, the emu forelimb fails to subsequently proliferate. The unique emu forelimb expression of Nkx2.5, previously associated with diminished wing development, initiates after this stage (concomitant with myoblast migration into the LPM) and is therefore unlikely to cause this developmental delay. In contrast, RNA sequencing of limb tissue reveals significantly lower Fgf10 expression in the emu forelimb. Artificially increasing Fgf10 expression in the emu LPM induces ectodermal Fgf8 expression and a limb bud. Analyzing open chromatin reveals differentially active regulatory elements near Fgf10 and Sall-1 in the emu wing, and the Sall-1 enhancer activity is dependent on a likely Fgf-mediated Ets transcription factor-binding site. Taken together, our results suggest that regulatory changes result in lower expression of Fgf10 and a concomitant failure to express genes required for limb proliferation in the early emu wing bud.

The multispecies coalescent (MSC) model provides a compelling framework for building phylogenetic trees from multilocus DNA sequence data. The pure MSC is best thought of as a special case of so-called “multispecies network coalescent” models, in which gene flow is allowed among branches of the tree, whereas MSC methods assume there is no gene flow between diverging species. Early implementations of the MSC, such as “parsimony” or “democratic vote” approaches to combining information from multiple gene trees, as well as concatenation, in which DNA sequences from multiple gene trees are combined into a single “supergene,” were quickly shown to be inconsistent in some regions of tree space, in so far as they converged on the incorrect species tree as more gene trees and sequence data were accumulated. The anomaly zone, a region of tree space in which the most frequent gene tree is different from the species tree, is one such region where many so-called “coalescent” methods are inconsistent. Second-generation implementations of the MSC employed Bayesian or likelihood models; these are consistent in all regions of gene tree space, but Bayesian methods in particular are incapable of handling the large phylogenomic data sets currently available. Two-step methods, such as MP-EST and ASTRAL, in which gene trees are first estimated and then combined to estimate an overarching species tree, are currently popular in part because they can handle large phylogenomic data sets. These methods are consistent in the anomaly zone but can sometimes provide inappropriate measures of tree support or apportion error and signal in the data inappropriately. MP-EST in particular employs a likelihood model which can be conveniently manipulated to perform statistical tests of competing species trees, incorporating the likelihood of the collected gene trees on each species tree in a likelihood ratio test. Such tests provide a useful alternative to the multilocus bootstrap, which only indirectly tests the appropriateness of competing species trees. We illustrate these tests and implementations of the MSC with examples and suggest that MSC methods are a useful class of models effectively using information from multiple loci to build phylogenetic trees.

In recent years, the field of sexual selection has exploded, with advances in theoretical and empirical research complementing each other in exciting ways. This perspective piece is the product of a “stock-taking” workshop on sexual selection and conflict. Our aim is to identify and deliberate on outstanding questions and to stimulate discussion rather than provide a comprehensive overview of the entire field. These questions are organized into four thematic sections we deem essential to the field. First we focus on the evolution of mate choice and mating systems. Variation in mate quality can generate both competition and choice in the opposite sex, with implications for the evolution of mating systems. Limitations on mate choice may dictate the importance of direct vs. indirect benefits in mating decisions and consequently, mating systems, especially with regard to polyandry. Second, we focus on how sender and receiver mechanisms shape signal design. Mediation of honest signal content likely depends on integration of temporally variable social and physiological costs that are challenging to measure. We view the neuroethology of sensory and cognitive receiver biases as the main key to signal form and the ‘aesthetic sense’ proposed by Darwin. Since a receiver bias is sufficient to both initiate and drive ornament or armament exaggeration, without a genetically correlated or even coevolving receiver, this may be the appropriate ‘null model’ of sexual selection. Thirdly, we focus on the genetic architecture of sexually selected traits. Despite advances in modern molecular techniques, the number and identity of genes underlying performance, display and secondary sexual traits remains largely unknown. In-depth investigations into the genetic basis of sexual dimorphism in the context of long-term field studies will reveal constraints and trajectories of sexually selected trait evolution. Finally, we focus on sexual selection and conflict as drivers of speciation. Population divergence and speciation are often influenced by an interplay between sexual and natural selection. The extent to which sexual selection promotes or counteracts population divergence may vary depending on the genetic architecture of traits as well as the covariance between mating competition and local adaptation. Additionally, post-copulatory processes, such as selection against heterospecific sperm, may influence the importance of sexual selection in speciation. We propose that efforts to resolve these four themes can catalyze conceptual progress in the field of sexual selection, and we offer potential avenues of research to advance this progress.

Natural history museums are unique spaces for interdisciplinary research and for educational innovation. Through extensive exhibits and public programming and by hosting rich communities of amateurs, students, and researchers at all stages of their careers, they provide a place-based window to focus on integration of science and discovery, as well as a locus for community engagement. At the same time, like a synthesis radio telescope, when joined together through emerging digital resources, the global community of museums (the ‘Global Museum’) is more than the sum of its parts, allowing insights and answers to diverse biological, environmental, and societal questions at the global scale, across eons of time, and spanning vast diversity across the Tree of Life. We argue that, whereas natural history collections and museums began with a focus on describing the diversity and peculiarities of species on Earth, they are now increasingly leveraged in new ways that significantly expand their impact and relevance. These new directions include the possibility to ask new, often interdisciplinary questions in basic and applied science; inform biomimetic design; and even provide solutions to climate change, global health and food security challenges. As institutions, they are incubators for cutting-edge research in biology and simultaneously protect core infrastructure for present and future societal needs. In this perspective, we discuss challenges to the realization of the full potential of natural history collections and museums to serve society. After reviewing collections and types of museums, including local and global efforts, we discuss the value of specimens and the importance of observations. We then focus on mapping and modelling of museum data (including place-based approaches and discovery), and explore the main projects, platforms and databases enabling this. We also explore ways in which improved infrastructure will allow higher quality science and increased opportunities for interdisciplinary research and communication, as well as new uses of collections. Finally, we aim to improve relevant protocols for the long-term storage of specimens and tissues, ensuring proper connection with tomorrow’s technologies and hence further increasing the relevance of natural history museums.