Publications

Population genetic theory and empirical evidence indicate that deleterious alleles can be purged in small populations. However, this viewpoint remains controversial. It is unclear whether natural selection is powerful enough to purge deleterious mutations when wild populations continue to decline. Pheasants are terrestrial birds facing a long-term risk of extinction as a result of anthropogenic perturbations and exploitation. Nevertheless, there are scant genomics resources available for conservation management and planning. Here, we analyzed comparative population genomic data for the three extant isolated populations of Brown eared pheasant (Crossoptilon mantchuricum) in China. We showed that C. mantchuricum has low genome-wide diversity and a contracting effective population size because of persistent declines over the past 100,000 years. We compared genome-wide variation in C. mantchuricum with that of its closely related sister species, the Blue eared pheasant (C. auritum) for which the conservation concern is low. There were detrimental genetic consequences across all C. mantchuricum genomes including extended runs of homozygous sequences, slow rates of linkage disequilibrium decay, excessive loss-of-function mutations, and loss of adaptive genetic diversity at the major histocompatibility complex region. To the best of our knowledge, this study is the first to perform a comprehensive conservation genomic analysis on this threatened pheasant species. Moreover, we demonstrated that natural selection may not suffice to purge deleterious mutations in wild populations undergoing long-term decline. The findings of this study could facilitate conservation planning for threatened species and help recover their population size.

Early events in the evolutionary history of a clade can shape the sensory systems of descendant lineages. Although the avian ancestor may not have had a sweet receptor, the widespread incidence of nectar-feeding birds suggests multiple acquisitions of sugar detection. In this study, we identify a single early sensory shift of the umami receptor (the T1R1-T1R3 heterodimer) that conferred sweet-sensing abilities in songbirds, a large evolutionary radiation containing nearly half of all living birds. We demonstrate sugar responses across species with diverse diets, uncover critical sites underlying carbohydrate detection, and identify the molecular basis of sensory convergence between songbirds and nectar-specialist hummingbirds. This early shift shaped the sensory biology of an entire radiation, emphasizing the role of contingency and providing an example of the genetic basis of convergence in avian evolution.

The diversity of genome sizes across the tree of life is of key interest in evolutionary biology. Various correlates of variation in genome size, such as accumulation of transposable elements (TEs) or rate of DNA gain and loss, are well known, but the underlying molecular mechanisms driving or constraining genome size are poorly understood. Here, we study one of the smallest genomes among frogs characterized thus far, that of the ornate burrowing frog (Platyplectrum ornatum) from Australia, and compare it to other published frog and vertebrate genomes to examine the forces driving reduction in genome size. At ∼1.06 gigabases (Gb), the P. ornatum genome is like that of birds, revealing four major mechanisms underlying TE dynamics: reduced abundance of all major classes of TEs; increased net deletion bias in TEs; drastic reduction in intron lengths; and expansion via gene duplication of the repertoire of TE-suppressing Piwi genes, accompanied by increased expression of Piwi-interacting RNA (piRNA)-based TE-silencing pathway genes in germline cells. Transcriptomes from multiple tissues in both sexes corroborate these results and provide insight into sex-differentiation pathways in Platyplectrum. Genome skimming of two closely related frog species (Lechriodus fletcheri and Limnodynastes fletcheri) confirms a reduction in TEs as a major driver of genome reduction in Platyplectrum and supports a macroevolutionary scenario of small genome size in frogs driven by convergence in life history, especially rapid tadpole development and tadpole diet. The P. ornatum genome offers a model for future comparative studies on mechanisms of genome size reduction in amphibians and vertebrates generally.

From 6 June to 20 August, 2020, I undertook a 76-day, ~3800 mile bicycle trip across the United States from the Atlantic to the Pacific oceans. In this talk I will share with you some of the amazing people, landscapes and birds I encountered, mostly in rural towns and along blue highways. The gradually changing birdscape, both in sight and sound, underscored the sensitive ecological gradients to which birds respond, as well as the ability of some species to thrive in agricultural monocultures. Rivers large and small regularly benchmarked my progress, as well as the western journey of Lewis & Clark over 200 years ago. The recent incidents in the US involving African Americans as targets of white violence inexorably caused me to festoon my bicycle with #BlackLivesMatter (#BLM) signs and share my experiences on social media. I encountered a variety of reactions, often positive and occasionally sharply negative, in a sea of generosity and extraordinary kindness as I wheeled my way through towns on the brink of collapse, vast private ranches and the occasional city. Rural America exhibits an abundance of loyalty and empathy for local communities, yet it is sometimes hard for Americans – myself included – to empathize with people they have never met in person. Two imperatives I took away, with ramifications for both biodiversity and political stability, were the need to somehow bring divergent communities together and to encourage empathy at the national level, among communities that otherwise experience each other only on TV.

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.