Vertebrate Tree Of Life Research Articles

Convergent genomic signatures associated with vertebrate viviparity

BackgroundViviparity—live birth—is a complex and innovative mode of reproduction that has evolved repeatedly across the vertebrate Tree of Life. Viviparous species exhibit remarkable levels of reproductive diversity, both in the amount of care provided by the parent during gestation, and the ways in which that care is delivered. The genetic basis of viviparity has garnered increasing interest over recent years; however, such studies are often undertaken on small evolutionary timelines, and thus are not able to address changes occurring on a broader scale. Using whole genome data, we investigated the molecular basis of this innovation across the diversity of vertebrates to answer a long held question in evolutionary biology: is the evolution of convergent traits driven by convergent genomic changes?ResultsWe reveal convergent changes in protein family sizes, protein-coding regions, introns, and untranslated regions (UTRs) in a number of distantly related viviparous lineages. Specifically, we identify 15 protein families showing evidence of contraction or expansion associated with viviparity. We additionally identify elevated substitution rates in both coding and noncoding sequences in several viviparous lineages. However, we did not find any convergent changes—be it at the nucleotide or protein level—common to all viviparous lineages.ConclusionsOur results highlight the value of macroevolutionary comparative genomics in determining the genomic basis of complex evolutionary transitions. While we identify a number of convergent genomic changes that may be associated with the evolution of viviparity in vertebrates, there does not appear to be a convergent molecular signature shared by all viviparous vertebrates. Ultimately, our findings indicate that a complex trait such as viviparity likely evolves with changes occurring in multiple different pathways.

Dollo-CDP: a polynomial-time algorithm for the clade-constrained large Dollo parsimony problem

The last decade of phylogenetics has seen the development of many methods that leverage constraints plus dynamic programming. The goal of this algorithmic technique is to produce a phylogeny that is optimal with respect to some objective function and that lies within a constrained version of tree space. The popular species tree estimation method ASTRAL, for example, returns a tree that (1) maximizes the quartet score computed with respect to the input gene trees and that (2) draws its branches (bipartitions) from the input constraint set. This technique has yet to be used for parsimony problems where the input are binary characters, sometimes with missing values. Here, we introduce the clade-constrained character parsimony problem and present an algorithm that solves this problem for the Dollo criterion score in O(|Sigma |^{3.726}(n+k) + |Sigma |^{1.726}nk) time, where n is the number of leaves, k is the number of characters, and Sigma is the set of clades used as constraints. Dollo parsimony, which requires traits/mutations to be gained at most once but allows them to be lost any number of times, is widely used for tumor phylogenetics as well as species phylogenetics, for example analyses of low-homoplasy retroelement insertions across the vertebrate tree of life. This motivated us to implement our algorithm in a software package, called Dollo-CDP, and evaluate its utility for analyzing retroelement insertion presence / absence patterns for bats, birds, toothed whales as well as simulated data. Our results show that Dollo-CDP can improve upon heuristic search from a single starting tree, often recovering a better scoring tree. Moreover, Dollo-CDP scales to data sets with much larger numbers of taxa than branch-and-bound while still having an optimality guarantee, albeit a more restricted one. Lastly, we show that our algorithm for Dollo parsimony can easily be adapted to Camin-Sokal parsimony but not Fitch parsimony.

Habitat split as a driver of disease in amphibians.

Anthropogenic habitat disturbance is fundamentally altering patterns of disease transmission and immunity across the vertebrate tree of life. Most studies linking anthropogenic habitat change and disease focus on habitat loss and fragmentation, but these processes often lead to a third process that is equally important: habitat split. Defined as spatial separation between the multiple classes of natural habitat that many vertebrate species require to complete their life cycles, habitat split has been linked to population declines in vertebrates, e.g. amphibians breeding in lowland aquatic habitats and overwintering in fragments of upland terrestrial vegetation. Here, we link habitat split to enhanced disease risk in amphibians (i) by reviewing the biotic and abiotic forces shaping elements of immunity and (ii) through a spatially oriented field study focused on tropical frogs. We propose a framework to investigate mechanisms by which habitat split influences disease risk in amphibians, focusing on three broad host factors linked to immunity: (i) composition of symbiotic microbial communities, (ii) immunogenetic variation, and (iii) stress hormone levels. Our review highlights the potential for habitat split to contribute to host-associated microbiome dysbiosis, reductions in immunogenetic repertoire, and chronic stress, that often facilitate pathogenic infections and disease in amphibians and other classes of vertebrates. We highlight that targeted habitat-restoration strategies aiming to connect multiple classes of natural habitats (e.g. terrestrial-freshwater, terrestrial-marine, marine-freshwater) could enhance priming of the vertebrate immune system through repeated low-load exposure to enzootic pathogens and reduced stress-induced immunosuppression.

Geographic and taxonomic biases in the vertebrate tree of life

AbstractAimResolving the tree of life is among the greatest challenges for modern biology, yet genetic data for many species are lacking to infer their position in the tree with confidence. In fact, little is known about what the missing species are and where to look for them. I identify main hotspots that host the most unsampled vertebrate species and test the hypothesis that local diversity determines the degree of sampling effort.LocationGlobal.TaxonTerrestrial vertebrates (amphibians, birds, mammals, reptiles).MethodsI use published distributional data and search DNA sequence repositories to identify taxa with no genetic data available. I map spatial patterns of the unsampled diversity and sampling effort to test the effect of species richness on sampling completeness. I examine the dependence of country‐level sampling completeness on the country's socio‐economic development.ResultsAbout 24% of living terrestrial vertebrate species have no genetic data available. The Andes, Central Africa and the Malay Archipelago are the most unsampled. Sampling effort is highest in North America, continental South‐East Asia and Amazonia. In contrast, Central Africa, the Horn of Africa, Malay Archipelago and Andes are consistently the least sampled regions. Regions of low diversity are better sampled than biodiversity hotspots.Main conclusionsThe most unsampled species are in the tropics. I pinpoint several key regions that are least represented in the tree of life and where sampling should be prioritized. Country's wealth seems to be an informative proxy for its sampling completeness.

Fossilized cell structures identify an ancient origin for the teleost whole-genome duplication

Teleost fishes comprise one-half of all vertebrate species and possess a duplicated genome. This whole-genome duplication (WGD) occurred on the teleost stem lineage in an ancient common ancestor of all living teleosts and is hypothesized as a trigger of their exceptional evolutionary radiation. Genomic and phylogenetic data indicate that WGD occurred in the Mesozoic after the divergence of teleosts from their closest living relatives but before the origin of the extant teleost groups. However, these approaches cannot pinpoint WGD among the many extinct groups that populate this 50- to 100-million-y lineage, preventing tests of the evolutionary effects of WGD. We infer patterns of genome size evolution in fossil stem-group teleosts using high-resolution synchrotron X-ray tomography to measure the bone cell volumes, which correlate with genome size in living species. Our findings indicate that WGD occurred very early on the teleost stem lineage and that all extinct stem-group teleosts known so far possessed duplicated genomes. WGD therefore predates both the origin of proposed key innovations of the teleost skeleton and the onset of substantial morphological diversification in the clade. Moreover, the early occurrence of WGD allowed considerable time for postduplication reorganization prior to the origin of the teleost crown group. This suggests at most an indirect link between WGD and evolutionary success, with broad implications for the relationship between genomic architecture and large-scale evolutionary patterns in the vertebrate Tree of Life.

Respiratory capacity is twice as important as temperature in explaining patterns of metabolic rate across the vertebrate tree of life.

Metabolic rate underlies a wide range of phenomena from cellular dynamics to ecosystem structure and function. Models seeking to statistically explain variation in metabolic rate across vertebrates are largely based on body size and temperature. Unexpectedly, these models overlook variation in the size of gills and lungs that acquire the oxygen needed to fuel aerobic processes. Here, we assess the importance of respiratory surface area in explaining patterns of metabolic rate across the vertebrate tree of life using a novel phylogenetic Bayesian multilevel modeling framework coupled with a species-paired dataset of metabolic rate and respiratory surface area. We reveal that respiratory surface area explains twice as much variation in metabolic rate, compared to temperature, across the vertebrate tree of life. Understanding the combination of oxygen acquisition and transport provides opportunity to understand the evolutionary history of metabolic rate and improve models that quantify the impacts of climate change.

The Evolution of Viviparity in Vertebrates.

In the vertebrate tree of life, viviparity or live birth has independently evolved many times, resulting in a rich diversity of reproductive strategies. Viviparity is believed to be a mode of reproduction that evolved from the ancestral condition of oviparity or egg laying, where most of the fetal development occurs outside the body. Today, there is not a simple model of parity transition to explain this species-specific divergence in modes of reproduction. Most evidence points to a gradual series of evolutionary adaptations that account for this phenomenon of reproduction, elegantly displayed by various viviparous squamates that exhibit placentae formed by the appositions of maternal and embryonic tissues, which share significant homology with the tissues that form the placenta in therian mammals. In an era where the genomes of many vertebrate species are becoming available, studies are now exploring the molecular basis of this transition from oviparity to viviparity, and in some rare instances its possible reversibility, such as the Australian three-toed skink (Saiphos equalis). In contrast to the parity diversity in squamates, mammals are viviparous with the notable exception of the egg-laying monotremes. Advancing computational tools coupled with increasing genome availability across species that utilize different reproductive strategies promise to reveal the molecular underpinnings of the ancestral transition of oviparity to viviparity. As a result, the dramatic changes in reproductive physiology and anatomy that accompany these parity changes can be reinterpreted. This chapter will briefly explore the vertebrate modes of reproduction using a phylogenetic framework and where possible highlight the role of potential candidate genes that may help explain the polygenic origins of live birth.

Heterogeneous relationships between rates of speciation and body size evolution across vertebrate clades.

Several theories predict that rates of phenotypic evolution should be related to the rate at which new lineages arise. However, drawing general conclusions regarding the coupling between these fundamental evolutionary rates has been difficult due to the inconsistent nature of previous results combined with uncertainty over the most appropriate methodology with which to investigate such relationships. Here we propose and compare the performance of several different approaches for testing associations between lineage-specific rates of speciation and phenotypic evolution using phylogenetic data. We then use the best-performing method to test relationships between rates of speciation and body size evolution in five major vertebrate clades (amphibians, birds, mammals, ray-finned fish and squamate reptiles) at two phylogenetic scales. Our results provide support for the long-standing view that rates of speciation and morphological evolution are generally positively related at broad macroevolutionary scales, but they also reveal a substantial degree of heterogeneity in the strength and direction of these associations at finer scales across the vertebrate tree of life.

Convergent Evolution of Elongate Forms in Craniates and of Locomotion in Elongate Squamate Reptiles.

Synopsis Elongate, snake- or eel-like, body forms have evolved convergently many times in most major lineages of vertebrates. Despite studies of various clades with elongate species, we still lack an understanding of their evolutionary dynamics and distribution on the vertebrate tree of life. We also do not know whether this convergence in body form coincides with convergence at other biological levels. Here, we present the first craniate-wide analysis of how many times elongate body forms have evolved, as well as rates of its evolution and reversion to a non-elongate form. We then focus on five convergently elongate squamate species and test if they converged in vertebral number and shape, as well as their locomotor performance and kinematics. We compared each elongate species to closely related quadrupedal species and determined whether the direction of vertebral or locomotor change matched in each case. The five lineages examined are obscure species from remote locations, providing a valuable glimpse into their biology. They are the skink lizards Brachymeles lukbani, Lerista praepedita, and Isopachys anguinoides, the basal squamate Dibamus novaeguineae, and the basal snake Malayotyphlops cf. ruficaudus. Our results support convergence among these species in the number of trunk and caudal vertebrae, but not vertebral shape. We also find that the elongate species are relatively slower than their limbed counterparts and move with lower frequency and higher amplitude body undulations, with the exception of Isopachys. This is among the first evidence of locomotor convergence across distantly related, elongate species.

Rapid decreases in relative testes mass among monogamous birds but not in other vertebrates.

Larger testes produce more sperm and therefore improve reproductive success in the face of sperm competition. Adaptation to social mating systems with relatively high and low sperm competition are therefore likely to have driven changes in relative testes size in opposing directions. Here, we combine the largest vertebrate testes mass dataset ever collected with phylogenetic approaches for measuring rates of morphological evolution to provide the first quantitative evidence for how relative testes mass has changed over time. We detect explosive radiations of testes mass diversity distributed throughout the vertebrate tree of life: bursts of rapid change have been frequent during vertebrate evolutionary history. In socially monogamous birds, there have been repeated rapid reductions in relative testes mass. We see no such pattern in other monogamous vertebrates; the prevalence of monogamy in birds may have increased opportunities for investment in alternative behaviours and physiologies allowing reduced investment in expensive testes.

The role of an overlooked adductor muscle in the feeding mechanism of ray-finned fishes: Predictions from simulations of a deep-sea viperfish

In a majority of ray-finned fishes (Actinopterygii), effective acquisition of food resources is predicated on rapid jaw adduction. Although the musculoskeletal architecture of the feeding system has been the subject of comparative research for many decades, individual contributions of the major adductor divisions to closing dynamics have not been elucidated. While it is understood that the dorsal divisions that arise from the head and insert on the posterior of the lower jaw are major contributors to closing dynamics, the contribution of the ventral components of the adductor system has been largely overlooked. In many ray-finned fishes, the ventral component is comprised of a single division, the Aω, that originates on an intersegmental aponeurosis of the facialis divisions and inserts on the medial face of the dentary, anterior to the Meckelian tendon. This configuration resembles a sling applied at two offset points of attachment on a third-order lever. The goal of this study was to elucidate the contributions of the Aω to jaw adduction by modeling jaw closing in the deep-sea viperfish Chauliodus sloani. To do this, we simulated adduction with a revised computational model that incorporates the geometry of the Aω. By comparing results between simulations that included and excluded Aω input, we show that the Aω adds substantially to lower-jaw adduction dynamics in C. sloani by acting as a steering motor and displacing the line of action of the dorsal facialis adductor muscles and increasing the mechanical advantage and input moment arms of the jaw lever system. We also explored the effect of the Aω on muscle dynamics and found that overall facialis muscle shortening velocities are higher and normalized force production is lower in simulations including the Aω. The net effect of these changes in muscle dynamics results in similar magnitudes of peak power in the facialis divisions between simulations, however, peak power is achieved earlier in adduction Modifications of muscle mechanics and posture result in significant increases in closing performance, including static bite force, angular velocity, and adduction time. We compare this configuration to a similar design in crocodilians and suggest that the Aω configuration and similar sling configurations across the vertebrate tree of life indicate the importance of this musculoskeletal design in feeding.

Early-branching euteleost relationships: areas of congruence between concatenation and coalescent model inferences.

Phylogenetic inference based on evidence from DNA sequences has led to significant strides in the development of a stable and robustly supported framework for the vertebrate tree of life. To date, the bulk of those advances have relied on sequence data from a small number of genome regions that have proven unable to produce satisfactory answers to consistently recalcitrant phylogenetic questions. Here, we re-examine phylogenetic relationships among early-branching euteleostean fish lineages classically grouped in the Protacanthopterygii using DNA sequence data surrounding ultraconserved elements. We report and examine a dataset of thirty-four OTUs with 17,957 aligned characters from fifty-three nuclear loci. Phylogenetic analysis is conducted in concatenated, joint gene trees and species tree estimation and summary coalescent frameworks. All analytical frameworks yield supporting evidence for existing hypotheses of relationship for the placement of Lepidogalaxias salamandroides, monophyly of the Stomiatii and the presence of an esociform + salmonid clade. Lepidogalaxias salamandroides and the Esociformes + Salmoniformes are successive sister lineages to all other euteleosts in the majority of analyses. The concatenated and joint gene trees and species tree analysis types produce high support values for this arrangement. However, inter-relationships of Argentiniformes, Stomiatii and Neoteleostei remain uncertain as they varied by analysis type while receiving strong and contradictory indices of support. Topological differences between analysis types are also apparent within the otomorph and the percomorph taxa in the data set. Our results identify concordant areas with strong support for relationships within and between early-branching euteleost lineages but they also reveal limitations in the ability of larger datasets to conclusively resolve other aspects of that phylogeny.

The Evolution of Energetic Scaling across the Vertebrate Tree of Life.

Metabolism is the link between ecology and physiology-it dictates the flow of energy through individuals and across trophic levels. Much of the predictive power of metabolic theories of ecology derives from the scaling relationship between organismal size and metabolic rate. There is growing evidence that this scaling relationship is not universal, but we have little knowledge of how it has evolved over macroevolutionary time. Here we develop a novel phylogenetic comparative method to investigate how often and in which clades the macroevolutionary dynamics of the metabolic scaling have changed. We find strong evidence that the metabolic scaling relationship has shifted multiple times across the vertebrate phylogeny. However, shifts are rare and otherwise strongly constrained. Importantly, both the estimated slope and intercept values vary widely across regimes, with slopes that spanned across theoretically predicted values such as 2/3 or 3/4. We further tested whether traits such as ecto-/endothermy, genome size, and quadratic curvature with body mass (i.e., energetic constraints at extreme body sizes) could explain the observed pattern of shifts. Though these factors help explain some of the variation in scaling parameters, much of the remaining variation remains elusive. Our results lay the groundwork for further exploration of the evolutionary and ecological drivers of major transitions in metabolic strategy and for harnessing this information to improve macroecological predictions.

Alternative adaptive immunity strategies: coelacanth, cod and shark immunity.

The advent of high throughput sequencing has permitted to investigate the genome and the transcriptome of novel non-model species with unprecedented depth. This technological advance provided a better understanding of the evolution of adaptive immune genes in gnathostomes, revealing several unexpected features in different fish species which are of particular interest. In the present paper, we review the current understanding of the adaptive immune system of the coelacanth, the elephant shark and the Atlantic cod. The study of coelacanth, the only living extant of the long thought to be extinct Sarcopterygian lineage, is fundamental to bring new insights on the evolution of the immune system in higher vertebrates. Surprisingly, coelacanths are the only known jawed vertebrates to lack IgM, whereas two IgD/W loci are present. Cartilaginous fish are of great interest due to their basal position in the vertebrate tree of life; the genome of the elephant shark revealed the lack of several important immune genes related to T cell functions, which suggest the existence of a primordial set of TH1-like cells. Finally, the Atlantic cod lacks a functional major histocompatibility II complex, but balances this evolutionary loss with the expansion of specific gene families, including MHC I, Toll-like receptors and antimicrobial peptides. Overall, these data point out that several fish species present an unconventional adaptive immune system, but the loss of important immune genes is balanced by adaptive evolutionary strategies which still guarantee the establishment of an efficient immune response against the pathogens they have to fight during their life.

The vertebrate taxonomy ontology: a framework for reasoning across model organism and species phenotypes.

BackgroundA hierarchical taxonomy of organisms is a prerequisite for semantic integration of biodiversity data. Ideally, there would be a single, expansive, authoritative taxonomy that includes extinct and extant taxa, information on synonyms and common names, and monophyletic supraspecific taxa that reflect our current understanding of phylogenetic relationships.DescriptionAs a step towards development of such a resource, and to enable large-scale integration of phenotypic data across vertebrates, we created the Vertebrate Taxonomy Ontology (VTO), a semantically defined taxonomic resource derived from the integration of existing taxonomic compilations, and freely distributed under a Creative Commons Zero (CC0) public domain waiver. The VTO includes both extant and extinct vertebrates and currently contains 106,947 taxonomic terms, 22 taxonomic ranks, 104,736 synonyms, and 162,400 cross-references to other taxonomic resources. Key challenges in constructing the VTO included (1) extracting and merging names, synonyms, and identifiers from heterogeneous sources; (2) structuring hierarchies of terms based on evolutionary relationships and the principle of monophyly; and (3) automating this process as much as possible to accommodate updates in source taxonomies.ConclusionsThe VTO is the primary source of taxonomic information used by the Phenoscape Knowledgebase (http://phenoscape.org/), which integrates genetic and evolutionary phenotype data across both model and non-model vertebrates. The VTO is useful for inferring phenotypic changes on the vertebrate tree of life, which enables queries for candidate genes for various episodes in vertebrate evolution.