Biology subjects

Gatesy, J.

Publications and source records attributed to Gatesy, J..

13 recordsLinked to original sources

bioRxiv2026

Ancient mitogenomes reveal unexpected diversity in Madagascar's extinct hippopotamuses

Madagascar's extinct hippopotamuses were a distinctive component of the island's recently lost megafauna, yet their origins, diversification history, and taxonomy have remained unresolved. Here, we recover the first ancient mitochondrial genomes from Malagasy hippopotamuses, obtaining phylogenetic data from 37 subfossil specimens across seven localities and all three named species, and integrate these data with morphology and total-evidence phylogenetic analyses. The 35 endemic specimens form a single clade most closely related to Hippopotamus amphibius, supporting a single colonization of Madagascar. Within this radiation, five deeply divergent and geographically structured mitochondrial lineages diversified across most regions of Madagascar during the Pleistocene. Tip-dating estimates a remarkably young crown age of ~1.41 Ma, following divergence from mainland Hippopotamus at ~3.24 Ma. These lineages do not map cleanly onto traditional taxonomy: material assigned to H. lemerleispans several divergent clades, while H. laloumena and H. madagascariensis are nested within this broader diversity. Morphology supports some lineage assignments but also points to previously unrecognized diversity, while ancestral-state reconstruction supports early body-size reduction followed by a secondary increase in H. laloumena. Malagasy hippopotamuses therefore represent an exceptionally recent radiation of large-bodied island mammals (and the youngest in Madagascar), showing that Madagascar continued to generate endemic mammalian diversity well into the Pleistocene. Their late-Holocene extinction erased the product of more than a million years of rapid insular diversification, the drivers of which remain enigmatic.

evolutionary biology↗

bioRxiv2025

Pseudogenes document protracted parallel regression of oral anatomy in myrmecophagous mammals

Adaptation to ant and/or termite consumption (myrmecophagy) in mammals constitutes a textbook example of convergent evolution, being independently derived in several mammalian lineages. Myrmecophagous species are characterized by striking convergent morphological adaptations such as skull elongation, enlargement of salivary glands, and long claws to dig into ant and termite nests. These evolutionary modifications also include anatomical regression, such as dental simplification or loss, reduction of masticatory muscles, and possessing a reduced set of taste buds. To gain insights into the molecular changes underlying the regression of these morpho-anatomical traits, we investigated the functionality of candidate genes related to dentition, gustation, and mastication in nine convergent myrmecophagous mammalian lineages. We examined these genes in a comparative phylogenetic context, paired with molecular evolutionary analyses, to estimate the relative timing of loss of gene function over the evolutionary history of each convergent lineage. We found that gustatory reduction and pseudogenization of masticatory myosin often were associated with the regression of dental genes. Evidence of pseudogenization events linked to oral anatomy dates to as early as the Cretaceous/Paleogene boundary, and is an ongoing process including examples of incipient gene inactivations. Whereas we found evidence for gene inactivations across all three functional categories occurring during distinct temporal intervals, there was variation in the sets of genes lost and the relative timing of inactivation events. The combined evidence suggests that the convergent evolution of myrmecophagy has occurred as a protracted process with distinct phases of anatomical evolution, over timescales as long as 60 Myr.

evolutionary biology↗

bioRxiv2023

Evolutionary constraint and innovation across hundreds of placental mammals

Evolutionary constraint and acceleration are powerful, cell-type agnostic measures of functional importance. Previous studies in mammals were limited by species number and reliance on human-referenced alignments. We explore the evolution of placental mammals, including humans, through reference-free whole-genome alignment of 240 species and protein-coding alignments for 428 species. We estimate 10.7% of the human genome is evolutionarily constrained. We resolve constraint to single nucleotides, pinpointing functional positions, and refine and expand by over seven-fold the catalog of ultraconserved elements. Overall, 48.5% of constrained bases are as yet unannotated, suggesting yet-to-be-discovered functional importance. Using species-level phenotypes and an updated phylogeny, we associate coding and regulatory variation with olfaction and hibernation. Focusing on biodiversity conservation, we identify genomic metrics that predict species at risk of extinction.

genomics↗

bioRxiv2022

A genomic timescale for placental mammal evolution

The precise pattern and timing of speciation events that gave rise to all living placental mammals remain controversial. We provide a comprehensive phylogenetic analysis of genetic variation across an alignment of 241 placental mammal genome assemblies, addressing prior concerns regarding limited genomic sampling across species. We compared neutral genome-wide phylogenomic signal using concatenation and coalescent-based approaches, interrogated phylogenetic variation across chromosomes and analyzed extensive catalogs of structural variants. Interordinal relationships exhibit relatively low rates of phylogenomic conflict across diverse datasets and analytical methods. Conversely, X-chromosome versus autosome conflicts characterize multiple independent clades that radiated during the Cenozoic. Genomic timetrees reveal an accumulation of cladogenic events before and immediately following the KPg boundary implying important roles for Cretaceous continental vicariance and the KPg extinction in the placental radiation. One-Sentence SummaryA comprehensive whole genome phylogeny of extant placental mammals reveals timing and patterns of ordinal diversification.

evolutionary biology↗

bioRxiv2022

Anatomical, ontogenetic, and genomic homologies guide reconstructions of the teeth-to-baleen transition in mysticete whales

The transition in Mysticeti (Cetacea) from capture of individual prey using teeth to bulk filtering batches of small prey using baleen ranks among the most dramatic evolutionary transformations in mammalian history. We review phylogenetic work on the homology of mysticete feeding structures from anatomical, ontogenetic, and genomic perspectives. Six characters with key functional significance for filter-feeding behavior are mapped to cladograms based on 11 morphological datasets to reconstruct evolutionary change across the teeth-to-baleen transition. This comparative summary within a common parsimony framework reveals extensive conflicts among independent systematic efforts but also broad support for the newly named clade Kinetomenta (Aetiocetidae + Chaeomysticeti). Complementary anatomical studies using CTscans and ontogenetic series hint at commonalities between the developmental programs for teeth and baleen, lending further support for a transitional chimaeric feeder scenario that best explains current knowledge on the transition to filter feeding. For some extant mysticetes, the ontogenetic sequence in fetal specimens recapitulates the inferred evolutionary transformation: from teeth, to teeth and baleen, to just baleen. Phylogenetic mapping of inactivating mutations reveals mutational decay of dental genes related to enamel formation before the emergence of crown Mysticeti, while baleen genes that were repurposed or newly derived during the evolutionary elaboration of baleen currently are poorly characterized. Review and meta-analysis of available data suggest that the teeth-to-baleen transition in Mysticeti ranks among the best characterized macroevolutionary shifts due to the diversity of data from the genome, the fossil record, comparative anatomy, and ontogeny that directly bears on this remarkable evolutionary transformation.

evolutionary biology↗

bioRxiv2022

Iterative deletion of gene trees detects extreme biases in distance-based phylogenomic coalescent analyses

Summary coalescent methods offer an alternative to the concatenation (supermatrix) approach for inferring phylogenetic relationships from genome-scale datasets. Given huge datasets, broad congruence between contrasting phylogenomic paradigms is often obtained, but empirical studies commonly show some well supported conflicts between concatenation and coalescence results and also between species trees estimated from alternative coalescent methods. Partitioned support indices can help arbitrate these discrepancies by pinpointing outlier loci that are unjustifiably influential at conflicting nodes. Partitioned coalescence support (PCS) recently was developed for summary coalescent methods, such as ASTRAL and MP-EST, that use the summed fits of individual gene trees to estimate the species tree. However, PCS cannot be implemented when distance-based coalescent methods (e.g., STAR, NJst, ASTRID, STEAC) are applied. Here, this deficiency is addressed by automating computation of partitioned coalescent branch length (PCBL), a novel index that uses iterative removal of individual gene trees to assess the impact of each gene on every clade in a distance-based coalescent tree. Reanalyses of five phylogenomic datasets show that PCBL for STAR and NJst trees helps quantify the overall stability/instability of clades and clarifies disagreements with results from optimality-based coalescent analyses. PCBL scores reveal severe missing taxa, apical nesting, misrooting, and basal dragdown biases. Contrived examples demonstrate the gross overweighting of outlier gene trees that drives these biases. Because of interrelated biases revealed by PCBL scores, caution should be exercised when using STAR and NJst, in particular when many taxa are analyzed, missing data are non-randomly distributed, and widespread gene-tree reconstruction error is suspected. Similar biases in the optimality-based coalescent method MP-EST indicate that congruence among species trees estimated via STAR, NJst, and MP-EST should not be interpreted as independent corroboration for phylogenetic relationships. Such agreements among methods instead might be due to the common defects of all three summary coalescent methods.

evolutionary biology↗

bioRxiv2021

Molecular Evolutionary Analyses of Tooth Genes Support Sequential Loss of Enamel and Teeth in Baleen Whales (Mysticeti)

The loss of teeth and evolution of baleen racks in Mysticeti was a profound transformation that permitted baleen whales to radiate and diversify into a previously underutilized ecological niche of bulk filter-feeding on zooplankton and other small prey. Ancestral state reconstructions suggest that teeth were lost in the common ancestor of crown Mysticeti. Genomic studies provide some support for this hypothesis and suggest that the genetic toolkit for enamel production was inactivated in the common ancestor of living baleen whales. However, molecular studies to date have not provided direct evidence for the complete loss of teeth, including their dentin component, on the stem mysticete branch. Given these results, several questions remain unanswered: (1) Were teeth lost in a single step or did enamel loss precede dentin loss? (2) Was enamel lost early or late on the stem mysticete branch? (3) If enamel and dentin/tooth loss were decoupled in the ancestry of baleen whales, did dentin loss occur on the stem mysticete branch or independently in different crown mysticete lineages? To address these outstanding questions, we compiled and analyzed complete protein-coding sequences for nine tooth-related genes from cetaceans with available genome data. Seven of these genes are associated with enamel formation (ACP4, AMBN, AMELX, AMTN, ENAM, KLK4, MMP20) whereas two other genes are either dentin-specific (DSPP) or tooth-specific (ODAPH) but not enamel-specific. Molecular evolutionary analyses indicate that all seven enamel-specific genes have inactivating mutations that are scattered across branches of the mysticete tree. Three of the enamel genes (ACP4, KLK4, MMP20) have inactivating mutations that are shared by all mysticetes. The two genes that are dentin-specific (DSPP) or tooth-specific (ODAPH) do not have any inactivating mutations that are shared by all mysticetes, but there are shared mutations in Balaenidae as well as in Plicogulae (Neobalaenidae + Balaenopteroidea). These shared mutations suggest that teeth were lost at most two times. Shared inactivating mutations and dN/dS analyses, in combination with cetacean divergence times, were used to estimate inactivation times of genes and by proxy enamel and tooth phenotypes. The results of these analyses are most compatible with a two-step model for the loss of teeth in the ancestry of living baleen whales: enamel was lost very early on the stem Mysticeti branch followed by the independent loss of dentin (and teeth) in the common ancestors of Balaenidae and Plicogulae, respectively. These results imply that some stem mysticetes, and even early crown mysticetes, may have had vestigial teeth comprised of dentin with no enamel. Our results also demonstrate that all odontocete species (in our study) with absent or degenerative enamel have inactivating mutations in one or more of their enamel genes.

evolutionary biology↗

bioRxiv2020

Genomic and anatomical comparisons of skin support independent adaptation to life in water by cetaceans and hippos

The macroevolutionary transition from terra firma to obligatory inhabitance of the marine hydrosphere has occurred twice in the history of Mammalia: Cetacea and Sirenia. In the case of Cetacea (whales, dolphins, porpoises), molecular phylogenies provide unambiguous evidence that fully aquatic cetaceans and semiaquatic hippopotamids (hippos) are each others closest living relatives. Ancestral reconstructions further suggest that some adaptations to the aquatic realm evolved in the common ancestor of Cetancodonta (Cetacea+Hippopotamidae). An alternative hypothesis is that these adaptations evolved independently in cetaceans and hippos. Here, we focus on the integumentary system and evaluate these hypotheses by integrating new histological data for cetaceans and hippos, the first genome-scale data for pygmy hippopotamus, and comprehensive genomic screens and molecular evolutionary analyses for protein-coding genes that have been inactivated in hippos and cetaceans. We identified ten skin-related genes that are inactivated in both cetaceans and hippos, including genes that are related to sebaceous glands, hair follicles, and epidermal differentiation. However, none of these genes exhibit inactivating mutations that are shared by cetaceans and hippos. Mean dates for the inactivation of skin genes in these two clades serve as proxies for phenotypic changes and suggest that hair reduction/loss, the loss of sebaceous glands, and changes to the keratinization program occurred ~16 million years earlier in cetaceans (~46.5 Ma) than in hippos (~30.5 Ma). These results, together with histological differences in the integument and prior analyses of oxygen isotopes from stem hippopotamids ("anthracotheres"), support the hypothesis that aquatic adaptations evolved independently in hippos and cetaceans.

evolutionary biology↗

bioRxiv2020

ILS-Aware Analyses of Retroelement Insertions in the Anomaly Zone

A potential shortcoming of concatenation methods for species tree estimation is their failure to account for incomplete lineage sorting. Coalescent methods address this problem but make various assumptions that, if violated, can result in worse performance than concatenation. Given the challenges of analyzing DNA sequences with both concatenation and coalescent methods, retroelement insertions (RIs) have emerged as powerful phylogenomic markers for species tree estimation. Here, we show that two recently proposed quartet-based methods, SDPquartets and ASTRAL BP, are statistically consistent estimators of the unrooted species tree topology under the coalescent when RIs follow a neutral infinite-sites model of mutation and the expected number of new RIs per generation is constant across the species tree. The accuracy of these (and other) methods for inferring species trees from RIs has yet to be assessed on simulated data sets, where the true species tree topology is known. Therefore, we evaluated eight methods given RIs simulated from four model species trees, all of which have short branches and at least three of which are in the anomaly zone. In our simulation study, ASTRAL BP and SDPquartets always recovered the correct species tree topology when given a sufficiently large number of RIs, as predicted. A distance-based method (ASTRID BP) and Dollo parsimony also performed well in recovering the species tree topology. In contrast, unordered, polymorphism, and Camin-Sokal parsimony typically fail to recover the correct species tree topology in anomaly zone situations with more than four ingroup taxa. Of the methods studied, only ASTRAL BP automatically estimates internal branch lengths (in coalescent units) and support values (i.e. local posterior probabilities). We examined the accuracy of branch length estimation, finding that estimated lengths were accurate for short branches but upwardly biased otherwise. This led us to derive the maximum likelihood (branch length) estimate for when RIs are given as input instead of binary gene trees; this corrected formula produced accurate estimates of branch lengths in our simulation study, provided that a sufficiently large number of RIs were given as input. Lastly, we evaluated the impact of data quantity on species tree estimation by repeating the above experiments with input sizes varying from 100 to 100 000 parsimony-informative RIs. We found that, when given just 1 000 parsimony-informative RIs as input, ASTRAL BP successfully reconstructed major clades (i.e clades separated by branches > 0.3 CUs) with high support and identified rapid radiations (i.e. shorter connected branches), although not their precise branching order. The local posterior probability was effective for controlling false positive branches in these scenarios.

evolutionary biology↗

bioRxiv2019

An ABBA-BABA Test for Introgression Using Retroposon Insertion Data

DNA sequence alignments provide the majority of data for inferring phylogenetic relationships with both concatenation and coalescence methods. However, DNA sequences are susceptible to extensive homoplasy, especially for deep divergences in the Tree of Life. Retroposon insertions have emerged as a powerful alternative to sequences for deciphering evolutionary relationships because these data are nearly homoplasy-free. In addition, retroposon insertions satisfy the no intralocus recombination assumption of summary coalescence methods because they are singular events and better approximate neutrality relative to DNA sequences commonly applied in phylogenomic work. Retroposons have traditionally been analyzed with phylogenetic methods that ignore incomplete lineage sorting (ILS). Here, we analyze three retroposon data sets for mammals (Placentalia, Laurasiatheria, Balaenopteroidea) with two different ILS-aware methods. The first approach constructs a species tree from retroposon bipartitions with ASTRAL, and the second is a modification of SVD-Quartets. We also develop a {chi}2 Quartet-Asymmetry Test to detect hybridization using retroposon data. Both coalescence methods recovered the same topology for each of the three data sets. The ASTRAL species tree for Laurasiatheria has consecutive short branch lengths that are consistent with an anomaly zone situation. For the Balaenopteroidea data set, which includes rorquals (Balaenopteridae) and gray whale (Eschrichtiidae), both coalescence methods recovered a topology that supports the paraphyly of Balaenopteridae. Application of the {chi}2 Quartet-Asymmetry Test to this data set detected 16 different quartets of species for which historical hybridization may be inferred, but significant asymmetry was not detected in the placental root and Laurasiatheria analyses.

evolutionary biology↗

bioRxiv2019

Retroposon Insertions within a Multispecies Coalescent Framework Suggest that Ratite Phylogeny is not in the ‘Anomaly Zone’

Summary coalescence methods were developed to address the negative impacts of incomplete lineage sorting on species tree estimation with concatenation. Coalescence methods are statistically consistent if certain requirements are met including no intralocus recombination, neutral evolution, and no gene tree reconstruction error. However, the assumption of no intralocus recombination may not hold for many DNA sequence data sets, and neutral evolution is not the rule for genetic markers that are commonly employed in phylogenomic coalescence analyses. Most importantly, the assumption of no gene tree reconstruction error is routinely violated, especially for rapid radiations that are deep in the Tree of Life. With the sequencing of complete genomes and novel pipelines, phylogenetic analysis of retroposon insertions has emerged as a valuable alternative to sequence-based phylogenetic analysis. Retroposon insertions avoid or reduce several problems that beset analysis of sequence data with summary coalescence methods: 1) intralocus recombination is avoided because retroposon insertions are singular evolutionary events, 2) neutral evolution is approximated in many cases, and 3) gene tree reconstruction errors are rare because retroposons have low rates of homoplasy. However, the analysis of retroposons within a multispecies coalescent framework has not been realized. Here, we propose a simple workaround in which a retroposon insertion matrix is first transformed into a series of incompletely resolved gene trees. Next, the program ASTRAL is used to estimate a species tree in the statistically consistent framework of the multispecies coalescent. The inferred species tree includes support scores at all nodes and internal branch lengths in coalescent units. As a test case, we analyzed a retroposon dataset for palaeognath birds (ratites and tinamous) with ASTRAL and compared the resulting species tree to an MP-EST species tree for the same clade derived from thousands of sequence-based gene trees. The MP-EST species tree suggests an empirical case of the anomaly zone with three very short internal branches at the base of Palaeognathae, and as predicted for anomaly zone conditions, the MP-EST species tree differs from the most common gene tree. Although identical in topology to the MP-EST tree, the ASTRAL species tree based on retroposons shows branch lengths that are much longer and incompatible with anomaly zone conditions. Simulation of gene trees from the retroposon-based species tree reveals that the most common gene tree matches the species tree. We contend that the wide discrepancies in branch lengths between sequence-based and retroposon-based species trees are explained by the greater accuracy of retroposon gene trees (bipartitions) relative to sequence-based gene trees. Coalescence analysis of retroposon data provides a promising alternative to the status quo by reducing gene tree reconstruction error that can have large impacts on both branch length estimates and evolutionary interpretations.

evolutionary biology↗

bioRxiv2019

Genes lost during the transition from land to water in cetaceans highlight genomic changes involved in aquatic adaptations

The transition from land to water in whales and dolphins (cetaceans) was accompanied by remarkable anatomical, physiological and behavioral adaptations. To better understand the genomic changes that occurred during this transition, we systematically screened for protein-coding genes that were inactivated in the ancestral cetacean lineage. We discovered genes whose loss is likely beneficial for cetaceans by reducing the risk of thrombus formation during diving (F12, KLKB1), improving the fidelity of oxidative DNA damage repair (POLM), and protecting from oxidative stress-induced lung inflammation (MAP3K19). Additional gene losses may reflect other diving-related adaptations, such as enhanced vasoconstriction during the diving response (mediated by SLC6A18) and altered pulmonary surfactant composition (SEC14L3), while loss of SLC4A9 relates to a reduced need for saliva in aquatic environments. Finally, the complete loss of melatonin synthesis and receptor genes (AANAT, ASMT, MTNR1A/B) may have been a precondition for the evolution of unihemispheric sleep. Our findings suggest that some genes lost in the ancestral cetacean lineage may have been involved in adapting to a fully-aquatic lifestyle.

evolutionary biology↗

bioRxiv2018

Partitioned coalescence support reveals biases in species-tree methods and detects gene trees that determine phylogenomic conflicts

Genomic datasets sometimes support unconventional or conflicting phylogenetic relationships when different tree-building methods are applied. Coherent interpretations of such results are enabled by partitioning support for controversial relationships among the constituent genes of a phylogenomic dataset. For the supermatrix (= concatenation) approach, several simple methods that measure the distribution of support and conflict among loci were introduced over 15 years ago. More recently, partitioned coalescence support (PCS) was developed for phylogenetic coalescence methods that account for incomplete lineage sorting and use the summed fits of gene trees to estimate the species tree. Here, we automate computation of PCS to permit application of this index to genome-scale matrices that include hundreds of loci. Reanalyses of four phylogenomic datasets for amniotes, land plants, skinks, and angiosperms demonstrate how PCS scores can be used to: 1) compare conflicting results favored by alternative coalescence methods, 2) identify outlier gene trees that have a disproportionate influence on the resolution of contentious relationships, 3) assess the effects of missing data in species-trees analysis, and 4) clarify biases in commonly-implemented coalescence methods and support indices. We show that key phylogenomic conclusions from these analyses often hinge on just a few gene trees and that results can be driven by specific biases of a particular coalescence method and/or the extreme weight placed on gene trees with high taxon sampling. Attributing exceptionally high weight to some gene trees and very low weight to other gene trees counters the basic logic of phylogenomic coalescence analysis; even clades in species trees with high support according to commonly used indices (likelihood-ratio test, bootstrap, Bayesian local posterior probability) can be unstable to the removal of only one or two gene trees with high PCS. Computer simulations cannot adequately describe all of the contingencies and complexities of empirical genetic data. PCS scores complement simulation work by providing specific insights into a particular dataset given the assumptions of the phylogenetic coalescence method that is applied. In combination with standard measures of nodal support, PCS provides a more complete understanding of the overall genomic evidence for contested evolutionary relationships in species trees.

evolutionary biology↗