Publications

2023
Gemmell P, Sackton TB, Edwards SV, Liu JS. A phylogenetic method linking nucleotide substitution rates to rates of continuous trait evolution. bioRxiv. 2023. Publisher's VersionAbstract
Genomes contain conserved non-coding sequences that perform important biological functions, such as gene regulation. We present a phylogenetic method, PhyloAcc-C, that associates nucleotide substitution rates with changes in a continuous trait of interest. The method takes as input a multiple sequence alignment of conserved elements, continuous trait data observed in extant species, and a background phylogeny and substitution process. Gibbs sampling is used to assign rate categories (background, conserved, accelerated) to lineages and explore whether the assigned rate categories are associated with increases or decreases in the rate of trait evolution. We test our method using simulations and then illustrate its application using mammalian body size and lifespan data previously analyzed with respect to protein coding genes. Like other studies, we find processes such as tumor suppression, telomere maintenance, and p53 regulation to be related to changes in longevity and body size. In addition, we also find that skeletal genes, and developmental processes, such as sprouting angiogenesis, are relevant. The R/C++ software package implementing our method is available under an open source license from https://github.com/phyloacc/PhyloAcc-C.
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Minias P, Edwards SV, Babik W. Ancient duplication, coevolution, and selection at the MHC class IIA and IIB genes of birds. Frontiers in Immunology. 2023 :1250824. Publisher's Version PDF
Yan H, Hu Z, Thomas GWC, Edwards SV, Sackton TB, Liu JS. PhyloAcc-GT: A Bayesian method for inferring patterns of substitution rate shifts on targeted lineages accounting for gene tree discordance. Molecular Biology and Evolution. 2023;40 (9) :msad195. Publisher's VersionAbstract
An important goal of evolutionary genomics is to identify genomic regions whose substitution rates differ among lineages. For example, genomic regions experiencing accelerated molecular evolution in some lineages may provide insight into links between genotype and phenotype. Several comparative genomics methods have been developed to identify genomic accelerations between species, including a Bayesian method called PhyloAcc, which models shifts in substitution rate in multiple target lineages on a phylogeny. However, few methods consider the possibility of discordance between the trees of individual loci and the species tree due to incomplete lineage sorting, which might cause false positives. Here, we present PhyloAcc-GT, which extends PhyloAcc by modeling gene tree heterogeneity. Given a species tree, we adopt the multispecies coalescent model as the prior distribution of gene trees, use Markov chain Monte Carlo (MCMC) for inference, and design novel MCMC moves to sample gene trees efficiently. Through extensive simulations, we show that PhyloAcc-GT outperforms PhyloAcc and other methods in identifying target lineage-specific accelerations and detecting complex patterns of rate shifts, and is robust to specification of population size parameters. PhyloAcc-GT is usually more conservative than PhyloAcc in calling convergent rate shifts because it identifies more accelerations on ancestral than on terminal branches. We apply PhyloAcc-GT to two examples of convergent evolution: flightlessness in ratites and marine mammal adaptations, and show that PhyloAcc-GT is a robust tool to identify shifts in substitution rate associated with specific target lineages while accounting for incomplete lineage sorting.
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Hill P, Dickman CR, Dinnage R, Duncan RP, Edwards SV, Greenville A, Sarre SD, Stringer EJ, Wardle GM, Gruber B. Episodic population fragmentation and gene flow reveal a trade-off between heterozygosity and allelic richness. Molecular Ecology. 2023. Publisher's VersionAbstract
In episodic environments like deserts, populations of some animal species exhibit irregular fluctuations such that populations are alternately large and connected or small and isolated. Such dynamics are typically driven by periodic resource pulses due, for example, to large but infrequent rainfall events. The repeated population bottlenecks resulting from fragmentation should lower genetic diversity over time, yet species undergoing these fluctuations appear to maintain high levels of genetic diversity. To resolve this apparent paradox, we simulated a metapopulation of constant size undergoing repeat episodes of fragmentation and change in gene flow to mimic outcomes experienced by mammals in an Australian desert. We show that episodic fragmentation and gene flow have contrasting effects on two measures of genetic diversity: heterozygosity and allelic richness. Specifically, fragmentation into many, small subpopulations, coupled with periods of infrequent gene flow, preserves allelic richness at the expense of heterozygosity. In contrast, fragmentation into a few, large subpopulations maintains heterozygosity at the expense of allelic richness. The strength of the trade-off between heterozygosity and allelic richness depends on the amount of gene flow and the frequency of gene flow events. Our results imply that the type of genetic diversity maintained among species living in strongly fluctuating environments will depend on the way populations fragment, with our results highlighting different mechanisms for maintaining allelic richness and heterozygosity in small, fragmented populations.
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Sadanandan KR, Ko M-C, Low GW, Gahr M, Edwards SV, Hiller M, Sackton TB, Rheindt FE, Sin SYW, Baldwin MW. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences. 2023;120 (43) :e2307340120. Publisher's VersionAbstract
Echolocation, the detection of objects by means of sound waves, has evolved independently in diverse animals. Echolocators include not only mammals such as toothed whales and yangochiropteran and rhinolophoid bats but also Rousettus fruit bats, as well as two bird lineages, oilbirds and swiftlets. In whales and yangochiropteran and rhinolophoid bats, positive selection and molecular convergence has been documented in key hearing-related genes, such as prestin (SLC26A5), but few studies have examined these loci in other echolocators. Here, we examine patterns of selection and convergence in echolocation-related genes in echolocating birds and Rousettus bats. Fewer of these loci were under selection in Rousettus or birds compared with classically recognized echolocators, and elevated convergence (compared to outgroups) was not evident across this gene set. In certain genes, however, we detected convergent substitutions with potential functional relevance, including convergence between Rousettus and classic echolocators in prestin at a site known to affect hair cell electromotility. We also detected convergence between Yangochiroptera, Rhinolophidea, and oilbirds in TMC1, an important mechanosensory transduction channel in vertebrate hair cells, and observed an amino acid change at the same site within the pore domain. Our results suggest that although most proteins implicated in echolocation in specialized mammals may not have been recruited in birds or Rousettus fruit bats, certain hearing-related loci may have undergone convergent functional changes. Investigating adaptations in diverse echolocators will deepen our understanding of this unusual sensory modality.
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Kryukov AP, Kryukov KA, Collier K, Fang B, Edwards SV. Mitogenomics clarifies the position of the Nearctic magpies (Pica hudsonia and Pica nuttalli) within the Holarctic magpie radiation. Current Zoology. 2023 :zoad048. Publisher's VersionAbstract
Partial separation of a peripheral population may lead to its divergence and, potentially, speciation due to genetic drift followed by selection and geographic isolation. This process may cause taxonomic uncertainty because reproductive isolation in allopatry cannot be verified directly. The two Nearctic allopatric species of magpies (Aves, Corvidae: Pica) serve as a good example of these problems. The Black-billed magpie Pica hudsonia is widely distributed in North America, whereas the Yellow-billed Magpie Pica nuttalli is endemic to restricted range in California. Their relationships with Palearctic species have been little studied. We obtained complete mitochondrial genomes of both Nearctic magpie species, along with the Eurasian Magpie (Pica pica) and the Oriental Magpie (Pica serica), 20 mitogenomes in total. Phylogenetic analysis reveals a basal position of P. serica, and P. pica as a sister clade to the two Nearctic species. P. hudsonia and P. nuttalli form reciprocal monophyletic subclades, showing recent divergence between and within them. Our data show that the Nearctic magpie lineage diverged from the common ancestor with P. pica, with a single migration wave via the Beringia. Within the Nearctic, we hypothesize a peripatric mode of speciation among Pica taxa due to divergence and separation of the small marginal population in California below the Sierra-Nevada mountains. Diversifying amino acid substitutions in ND4-ND5-ND6 genes along the branch leading to the New World clade may indicate selection for heat-tolerance. Considering the clear phenotypic differences between P. hudsonia and P. nuttalli, our data, showing their reciprocal monophylies and genetic distinctness, is consistent with the two-species taxonomy.
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Huynh S, Cloutier A, Chen G, Tsz D, Chan C, Lam DKong, Huyvaert KP, Sato F, Edwards SV, Sin SYW. Whole-genome analyses reveal past population fluctuations and low genetic diversities of the North Pacific albatrosses. Molecular Biology and Evolution. 2023;40 (7) :msad155. Publisher's VersionAbstract
Throughout the Plio-Pleistocene, climate change has impacted tropical marine ecosystems substantially, with even more severe impacts predicted in the Anthropocene. Although many studies have clarified demographic histories of seabirds in polar regions, the history of keystone seabirds of the tropics is unclear, despite the prominence of albatrosses (Diomedeidae, Procellariiformes) as the largest and most threatened group of oceanic seabirds. To understand the impact of climate change on tropical albatrosses, we investigated the evolutionary and demographic histories of all four North Pacific albatrosses and their prey using whole-genome analyses. We report a striking concordance in demographic histories among the four species, with a notable dip in effective population size at the beginning of the Pleistocene and a population expansion in the Last Glacial Period when sea levels were low, which resulted in increased potential coastal breeding sites. Abundance of the black-footed albatross dropped again during the Last Glacial Maximum, potentially linked to climate-driven loss of breeding sites and concordant genome-derived decreases in its major prey. We find very low genome-wide (π < 0.001) and adaptative genetic diversities across the albatrosses, with genes of the major histocompatibility complex close to monomorphic. We also identify recent selective sweeps at genes associated with hyperosmotic adaptation, longevity, and cognition and memory. Our study has shed light on the evolutionary and demographic histories of the largest tropical oceanic seabirds and provides evidence for their large population fluctuations and alarmingly low genetic diversities.
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Liu L, Liu Y, Wu S, Arnold J, Whalen C, Davis C, Edwards SV. Short branch attraction in phylogenomic inference under the multispecies coalescent. Frontiers in Ecology and Evolution. 2023;11. Publisher's VersionAbstract
Accurate reconstruction of species trees often relies on the quality of input gene trees estimated from molecular sequences. Previous studies suggested that if the sequence length is fixed, the maximum likelihood may produce biased gene trees which subsequently mislead inference of species trees. Two key questions need to be answered in this context: what are the scenarios that may result in consistently biased gene trees? and for those scenarios, are there any remedies that may remove or at least reduce the misleading effects of consistently biased gene trees? In this article, we establish a theoretical framework to address these questions. Considering a scenario where the true gene tree is a 4-taxon star tree T SS SS ∗=() 1 234 ,, , with two short branches leading to the species S1 and S2, we demonstrate that maximum likelihood significantly favors the wrong bifurcating tree [(S1, S2), S3, S4] grouping the two species S1 and S2 with short branches. We name this inconsistent behavior short branch attraction, which may occur in real-world data involving a 4-taxon bifurcating gene tree with a short internal branch. If no mutation occurs along the internal branch, which is likely if the internal branch is short, the 4-taxon bifurcating tree is equivalent to the 4-taxon star tree and thus will suffer the same misleading effect of short branch attraction. Theoretical and simulation results further demonstrate that short branch attraction may occur in gene trees and species trees of arbitrary size. Moreover, short branch attraction is primarily caused by a lack of phylogenetic information in sequence data, suggesting that converting short internal branches to polytomies in the estimated gene trees can significantly reduce artifacts induced by short branch attraction. KEYWORDS coalescent methods, species trees, gene trees, multispecies coalescent model, long branch attraction, short branch attraction
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Lorente-Martinez H, Agorreta A, Irisarri I, Zardoya R, Edwards SV, San Mauro D. Multiple Instances of Adaptive Evolution in Aquaporins of Amphibious Fishes. Biology. 2023;12 (6) :846. Publisher's VersionAbstract

Aquaporins (AQPs) are a highly diverse family of transmembrane proteins involved in osmotic regulation that played an important role in the conquest of land by tetrapods. However, little is known about their possible implication in the acquisition of an amphibious lifestyle in actinopterygian fishes. Herein, we investigated the molecular evolution of AQPs in 22 amphibious actinopterygian fishes by assembling a comprehensive dataset that was used to (1) catalogue AQP paralog members and classes; (2) determine the gene family birth and death process; (3) test for positive selection in a phylogenetic framework; and (4) reconstruct structural protein models. We found evidence of adaptive evolution in 21 AQPs belonging to 5 different classes. Almost half of the tree branches and protein sites that were under positive selection were found in the AQP11 class. The detected sequence changes indicate modifications in molecular function and/or structure, which could be related to adaptation to an amphibious lifestyle. AQP11 orthologues appear to be the most promising candidates to have facilitated the processes of the water-to-land transition in amphibious fishes. Additionally, the signature of positive selection found in the AQP11b stem branch of the Gobiidae clade suggests a possible case of exaptation in this clade.

Keywords: 

aquaporinamphibious fishesadaptive evolutionemersion

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Khalil S, Enbody ED, Frankl-Vilches C, Welklin JF, Koch RE, Toomey MB, Sin SYW, Edwards SV, Gahr M, Schwabl H, et al. Testosterone coordinates gene expression across different tissues to produce carotenoid-based red ornamentation. Molecular Biology and Evolution. 2023;40 (4) :msad056. Publisher's VersionAbstract
Carotenoid pigments underlie most of the red, orange, and yellow visual signals used in mate choice in vertebrates. However, many of the underlying processes surrounding the production of carotenoid-based traits remain unclear due to the complex nature of carotenoid uptake, metabolism, and deposition across tissues. Here, we leverage the ability to experimentally induce the production of a carotenoid-based red plumage patch in the red-backed fairywren (Malurus melanocephalus), a songbird in which red plumage is an important male sexual signal. We experimentally elevated testosterone in unornamented males lacking red plumage to induce the production of ornamentation and compared gene expression in both the liver and feather follicles between unornamented control males, testosterone-implanted males, and naturally ornamented males. We show that testosterone upregulates the expression of CYP2J19, a gene known to be involved in ketocarotenoid metabolism, and a putative carotenoid processing gene (ELOVL6) in the liver, and also regulates the expression of putative carotenoid transporter genes in red feather follicles on the back, including ABCG1. In black feathers, carotenoid-related genes are downregulated and melanin genes upregulated, but we find that carotenoids are still present in the feathers. This may be due to the activity of the carotenoid-cleaving enzyme BCO2 in black feathers. Our study provides a first working model of a pathway for carotenoid-based trait production in free-living birds, implicates testosterone as a key regulator of carotenoid-associated gene expression, and suggests hormones may coordinate the many processes that underlie the production of these traits across multiple tissues.
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Burley JT, Orzechowski SCM, Sin SYW, Edwards SV. Whole‐genome phylogeography of the blue‐faced honeyeater (Entomyzon cyanotis) and discovery and characterization of a neo‐Z chromosome. Molecular Ecology. 2023;32 (6) :1248-1270. Publisher's VersionAbstract
Whole-genome surveys of genetic diversity and geographic variation often yield unexpected discoveries of novel structural variation, which long-read DNA sequencing can help clarify. Here, we report on whole-genome phylogeography of a bird exhibiting classic vicariant geographies across Australia and New Guinea, the blue-faced honeyeater (Entomyzon cyanotis), and the discovery and characterization of a novel neo-Z chromosome by long-read sequencing. Using short-read genome-wide SNPs, we inferred population divergence events within E. cyanotis across the Carpentarian and other biogeographic barriers during the Pleistocene (~0.3–1.7 Ma). Evidence for introgression between nonsister populations supports a hypothesis of reticulate evolution around a triad of dynamic barriers around Pleistocene Lake Carpentaria between Australia and New Guinea. During this phylogeographic survey, we discovered a large (134 Mbp) neo-Z chromosome and we explored its diversity, divergence and introgression landscape. We show that, as in some sylvioid passerine birds, a fusion occurred between chromosome 5 and the Z chromosome to form a neo-Z chromosome; and in E. cyanotis, the ancestral pseudoautosomal region (PAR) appears nonrecombinant between Z and W, along with most of the fused chromosome 5. The added recombination-suppressed portion of the neo-Z (~37.2 Mbp) displays reduced diversity and faster population genetic differentiation compared with the ancestral-Z. Yet, the new PAR (~17.4 Mbp) shows elevated diversity and reduced differentiation compared to autosomes, potentially resulting from introgression. In our case, long-read sequencing helped clarify the genomic landscape of population divergence on autosomes and sex chromosomes in a species where prior knowledge of genome structure was still incomplete.
Sin SYW, Ke F, Chen G, Guoling P-Y, Enbody E, Karubian J, Webster MS, Edwards SV. Genetic basis and evolution of structural color polymorphism in an Australian songbird. bioRxiv. 2023. Publisher's VersionAbstract
Island organisms often evolve phenotypes divergent from their mainland counterparts, providing a useful system for studying adaption under differential selection. Some island birds have melanic plumage differing from the color of mainland conspecifics, a trait proposed as an insular adaptation. In the white-winged fairywren (Malurus leucopterus), subspecies on two islands have a black nuptial plumage whereas the subspecies on the Australian mainland has a blue nuptial plumage. The black subspecies have a feather nanostructure that could produce a blue structural color, suggesting a blue ancestor. An earlier study proposed independent evolution of melanism on the islands based on the history of subspecies divergence. However, the genetic basis of melanism and the origin of color differentiation in this group are still unknown. Here, we used whole-genomes to investigate the genetic basis of melanism by comparing the blue and black M. leucopterus subspecies to identify highly divergent genomic regions. We identified a well-known pigmentation gene ASIP and four candidate genes that may contribute to feather nanostructure development. We also detected signatures of a selective sweep in genomic regions containing ASIP and SCUBE2 not in the black subspecies, as predicted by earlier work, but in the blue subspecies, which possesses many derived SNPs in these regions, suggesting that the mainland subspecies has re-evolved a blue plumage from a black ancestor. This re-evolution was likely driven by a pre-existing female preference. Our findings provide new insight into the evolution of plumage coloration in island versus continental populations, and, importantly, we identify candidate genes that likely play roles in the development and evolution of feather structural coloration.
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Card DC, W. Jennings B, Edwards SV. Genome Evolution and the Future of Phylogenomics of Non-Avian Reptiles . Animals. 2023;13 (2) :471. Publisher's VersionAbstract

Abstract

Non-avian reptiles comprise a large proportion of amniote vertebrate diversity, with squamate reptiles—lizards and snakes—recently overtaking birds as the most species-rich tetrapod radiation. Despite displaying an extraordinary diversity of phenotypic and genomic traits, genomic resources in non-avian reptiles have accumulated more slowly than they have in mammals and birds, the remaining amniotes. Here we review the remarkable natural history of non-avian reptiles, with a focus on the physical traits, genomic characteristics, and sequence compositional patterns that comprise key axes of variation across amniotes. We argue that the high evolutionary diversity of non-avian reptiles can fuel a new generation of whole-genome phylogenomic analyses. A survey of phylogenetic investigations in non-avian reptiles shows that sequence capture-based approaches are the most commonly used, with studies of markers known as ultraconserved elements (UCEs) especially well represented. However, many other types of markers exist and are increasingly being mined from genome assemblies in silico, including some with greater information potential than UCEs for certain investigations. We discuss the importance of high-quality genomic resources and methods for bioinformatically extracting a range of marker sets from genome assemblies. Finally, we encourage herpetologists working in genomics, genetics, evolutionary biology, and other fields to work collectively towards building genomic resources for non-avian reptiles, especially squamates, that rival those already in place for mammals and birds. Overall, the development of this cross-amniote phylogenomic tree of life will contribute to illuminate interesting dimensions of biodiversity across non-avian reptiles and broader amniotes.

Keywords: 

anonymous lociGC contentgenome sizeisochoreskaryotypenatural historyreduced representationrepetitive elementssex determination and chromosomestarget captureultraconserved elements

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Wu MYue, Forcina G, Low GWeijie, Sadanandan KR, Gwee CY, van Grouw H, Wu S, Edwards SV, Baldwin MW, Rheindt FE. Historic samples reveal loss of wild genotype through domestic chicken introgression during the Anthropocene. PLoS genetics. 2023;19 (1) :e1010551. Publisher's VersionAbstract
Human activities have precipitated a rise in the levels of introgressive gene flow among animals. The investigation of conspecific populations at different time points may shed light on the magnitude of human-mediated introgression. We used the red junglefowl Gallus gallus, the wild ancestral form of the chicken, as our study system. As wild junglefowl and domestic chickens readily admix, conservationists fear that domestic introgression into junglefowl may compromise their wild genotype. By contrasting the whole genomes of 51 chickens with 63 junglefowl from across their natural range, we found evidence of a loss of the wild genotype across the Anthropocene. When comparing against the genomes of junglefowl from approximately a century ago using rigorous ancient-DNA protocols, we discovered that levels of domestic introgression are not equal among and within modern wild populations, with the percentage of domestic ancestry around 20–50%. We identified a number of domestication markers in which chickens are deeply differentiated from historic junglefowl regardless of breed and/or geographic provenance, with eight genes under selection. The latter are involved in pathways dealing with development, reproduction and vision. The wild genotype is an allelic reservoir that holds most of the genetic diversity of Ggallus, a species which is immensely important to human society. Our study provides fundamental genomic infrastructure to assist in efforts to prevent a further loss of the wild genotype through introgression of domestic alleles.
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Edwards SV, Tonini JFR, Mcinerney N, Welch C, Beerli P. Multilocus phylogeography, population genetics and niche evolution of Australian brown and black-tailed treecreepers (Aves: Climacteris). Biological Journal of the Linnean Society. 2023;138 (3) :249-273. Publisher's VersionAbstract
The Carpentarian barrier across north-eastern Australia is a major biogeographic barrier and a generator of biodiversity within the Australian Monsoonal Tropics. Here we present a continent-wide analysis of mitochondrial (control region) and autosomal (14 anonymous loci) sequence and indel variation and niche modelling of brown and black-tailed treecreepers (Climacteris picumnus and Climacteris melanurus), a clade with a classic distribution on either side of the Carpentarian barrier. mtDNA control region sequences exhibited reciprocal monophyly and strong differentiation (Fst = 0.91), and revealed a signature of a recent selective sweep in C. picumnus. A variety of tests support an isolation-with-migration model of divergence, albeit with low levels of gene flow across the Carpentarian barrier and a divergence time between species of ~1.7–2.8 Mya. Palaeoecological niche models show that both range size as measured by available habitat and estimated historical population sizes of both species declined in the past ~600 kyr and that the area of interspecific range overlap was never historically large, perhaps decreasing opportunities for extensive gene flow. The relatively long divergence time and low opportunity for gene flow may have facilitated speciation more so than in other co-distributed bird taxa across the Australian Monsoonal Tropics.
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Blischak PD, Brown JM, Cao Z, Cloutier A, Cobb K, DiGiacomo AA, Eaton DAR, Edwards SV, Gallivan KA, Gates DJ, et al. Species Tree Inference: A Guide to Methods and Applications. Princeton: Princeton University Press; 2023. Publisher's VersionAbstract
An up-to-date reference book on phylogenetic methods and applications for evolutionary biologists The increasingly widespread availability of genomic data is transforming how biologists estimate evolutionary relationships among organisms and broadening the range of questions that researchers can test in a phylogenetic framework. Species Tree Inference brings together many of today’s leading scholars in the field to provide an incisive guide to the latest practices for analyzing multilocus sequence data. This wide-ranging and authoritative book gives detailed explanations of emerging new approaches and assesses their strengths and challenges, offering an invaluable context for gauging which procedure to apply given the types of genomic data and processes that contribute to differences in the patterns of inheritance across loci. It demonstrates how to apply these approaches using empirical studies that span a range of taxa, timeframes of diversification, and processes that cause the evolutionary history of genes across genomes to differ. By fully embracing this genomic heterogeneity, Species Tree Inference illustrates how to address questions beyond the goal of estimating phylogenetic relationships of organisms, enabling students and researchers to pursue their own research in statistically sophisticated ways while charting new directions of scientific discovery.
2022
Card DC, Shapiro B, Giribet G, Moritz C, Edwards SV. Museum Genomics. Annual Review of Genetics. 2022;55 :633-659. Publisher's VersionAbstract
Natural history collections are invaluable repositories of biological information that provide an unrivaled record of Earth's biodiversity. Museum genomics—genomics research using traditional museum and cryogenic collections and the infrastructure supporting these investigations—has particularly enhanced research in ecology and evolutionary biology, the study of extinct organisms, and the impact of anthropogenic activity on biodiversity. However, leveraging genomics in biological collections has exposed challenges, such as digitizing, integrating, and sharing collections data; updating practices to ensure broadly optimal data extraction from existing and new collections; and modernizing collections practices, infrastructure, and policies to ensure fair, sustainable, and genomically manifold uses of museum collections by increasingly diverse stakeholders. Museum genomics collections are poised to address these challenges and, with increasingly sensitive genomics approaches, will catalyze a future era of reproducibility, innovation, and insight made possible through integrating museum and genome sciences.
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Butler JM, McKinney J, Ludington SC, Mabogunje M, Singh D, Edwards SV, O'Connell LA. Development of the visual system in social poison frog tadpoles. bioRxiv. 2022. Publisher's VersionAbstract
The ways in which animals sense the world around them change throughout development. Young of many species have absent or limited visual capabilities, but still make complex decisions about individuals with whom they interact. Poison frog tadpoles display complex social behaviors that have been suggested to rely on vision despite a century of research indicating tadpoles have poorly-developed visual systems. Here, we examined visual system development in tadopoles of the Mimetic Poison Frog (Ranitomeya imitator) that use begging displays to stimulate egg feeding from their mothers. Neural activation in the retina increased in begging metamorphic tadpoles, but not in begging pre-metamorphic tadpoles. Molecular profiling of active eye neurons during begging identified numerous differentially expressed development-related transcripts, suggesting that developmental stage, not begging, was driving gene expression profiles. Using the neural tracer neurobiotin, we found that connections between the eye and brain proliferate during metamorphosis, with little retinotectal connections in recently-hatched tadpoles. To assess visual capabilities of tadpoles, we used a light/dark preference assay in early, middle, and late stages. All tadpoles showed a preference for the dark side, but the strength of preference increased with developmental stage and eyes were not required for this behavior. Taken together, these data indicate visual ontology of poison frog tadpoles is similar to that of other frogs, with poor visual capabilities at hatching and immense morphological and physiological changes occurring during metamorphosis. More broadly, this highlights the importance of multimodal cues, including photodetection via the pineal structure, in tadpole social interactions.
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Card DC, Van Camp AG, Santonastaso T, Jensen-Seaman MI, Anthony NM, Edwards SV. Structure and evolution of the squamate major histocompatibility complex as revealed by two Anolis lizard genomes. Frontiers in Genetics. 2022;13. Publisher's VersionAbstract
The major histocompatibility complex (MHC) is an important genomic region for adaptive immunity and has long been studied in ecological and evolutionary contexts, such as disease resistance and mate and kin selection. The MHC has been investigated extensively in mammals and birds but far less so in squamate reptiles, the third major radiation of amniotes. We localized the core MHC genomic region in two squamate species, the green anole (Anolis carolinensis) and brown anole (A. sagrei), and provide the first detailed characterization of the squamate MHC, including the presence and ordering of known MHC genes in these species and comparative assessments of genomic structure and composition in MHC regions. We find that the Anolis MHC, located on chromosome 2 in both species, contains homologs of many previously-identified mammalian MHC genes in a single core MHC region. The repetitive element composition in anole MHC regions was similar to those observed in mammals but had important distinctions, such as higher proportions of DNA transposons. Moreover, longer introns and intergenic regions result in a much larger squamate MHC region (11.7 Mb and 24.6 Mb in the green and brown anole, respectively). Evolutionary analyses of MHC homologs of anoles and other representative amniotes uncovered generally monophyletic relationships between species-specific homologs and a loss of the peptide-binding domain exon 2 in one of two mhc2β gene homologs of each anole species. Signals of diversifying selection in each anole species was evident across codons of mhc1, many of which appear functionally relevant given known structures of this protein from the green anole, chicken, and human. Altogether, our investigation fills a major gap in understanding of amniote MHC diversity and evolution and provides an important foundation for future squamate-specific or vertebrate-wide investigations of the MHC.
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McKinney J, Ludington SC, Mabogunje M, Singh D, Edwards SV, O'Connell LA. Development of the visual system in social poison frog tadpoles. bioRxiv. 2022. Publisher's VersionAbstract
The ways in which animals sense the world around them change throughout development. Young of many species have absent or limited visual capabilities, but still make complex decisions about individuals with whom they interact. Poison frog tadpoles display complex social behaviors that have been suggested to rely on vision despite a century of research indicating tadpoles have poorly-developed visual systems. Here, we examined visual system development in tadopoles of the Mimetic Poison Frog (Ranitomeya imitator) that use begging displays to stimulate egg feeding from their mothers. Neural activation in the retina increased in begging metamorphic tadpoles, but not in begging pre-metamorphic tadpoles. Molecular profiling of active eye neurons during begging identified numerous differentially expressed development-related transcripts, suggesting that developmental stage, not begging, was driving gene expression profiles. Using the neural tracer neurobiotin, we found that connections between the eye and brain proliferate during metamorphosis, with little retinotectal connections in recently-hatched tadpoles. To assess visual capabilities of tadpoles, we used a light/dark preference assay in early, middle, and late stages. All tadpoles showed a preference for the dark side, but the strength of preference increased with developmental stage and eyes were not required for this behavior. Taken together, these data indicate visual ontology of poison frog tadpoles is similar to that of other frogs, with poor visual capabilities at hatching and immense morphological and physiological changes occurring during metamorphosis. More broadly, this highlights the importance of multimodal cues, including photodetection via the pineal structure, in tadpole social interactions.
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