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Cunha, T. J.

Publications and source records attributed to Cunha, T. J..

5 recordsLinked to original sources

No silver bullet: Patterns of macrosynteny recapitulate systemic conflicts in the higher-level relationships of the arachnids

Rare genomic changes have long been sought by phylogeneticists for their potential to resolve obdurate nodes in the tree of life. Recently, patterns of macrosynteny have been proffered as a breakthrough for challenging relationships within invertebrates. One taxon that stands to benefit from the application of this approach is Chelicerata (the sister group to the rest of Arthropoda), whose radiation has long defied resolution, despite intensive investigations using morphological characters, molecular sequence data, and a combination thereof. Challenges to the resolution of chelicerate phylogeny include an ancient rapid radiation, the incidence of several fast-evolving lineages prone to long-branch attraction artifacts, and extinction of multiple ordinal level lineages that cannot be sampled for breaking long branches. At present, only a subset of nodes has been stably resolved. To break this impasse, we brought to bear multiple classes of phylogenetically informative rare genomic changes, including the sequencing of the first genomes for Ricinulei and Palpigradi. Here, we show that an ancient, shared whole genome duplication event is restricted to Arachnopulmonata (the most recent common ancestor of spiders and scorpions), disfavoring traditional placements of either Ricinulei or Palpigradi as close relatives of tetrapulmonates. Intriguingly, investigation of fusion-with-mixing events identified equal support for mutually exclusive placements for Acariformes, the least stable of the arachnid orders. Our results suggest that fusion-with-mixing, far from being a silver bullet, likely exhibits the same emergent property as all character systems, in that it is prone to homoplasy and conflicting signal stemming from ancient rapid radiations.

evolutionary biology↗

Global genomics of the man-o'-war (Physalia) reveal biodiversity at the ocean surface

The open ocean is a vast, highly connected environment, and the organisms found there have been hypothesized to represent massive, well-mixed populations. Of these, the Portuguese man-o-war (Physalia) is uniquely suited to dispersal, sailing the ocean surface with a muscular crest. We tested the hypothesis of a single, panmictic Physalia population by sequencing 133 genomes, and found five distinct lineages, with multiple lines of evidence showing strong reproductive isolation despite range overlap. We then scored thousands of citizen-science photos and identified four recognizable morphologies linked to these lineages. Within lineages, we detected regionally endemic subpopulations, connected by winds and currents, and identified individual long-distance dispersal events. We find that, even in these sailing species, genetic variation is highly partitioned geographically across the open ocean. SummaryThe open ocean is a vast and highly connected environment. The organisms that live there have a significant capacity for dispersal and few geographic boundaries to separate populations. Of these, the Portuguese man-o-war or bluebottle (genus Physalia) is uniquely suited to long-distance travel, using its gas-filled float and muscular crest to catch the wind and sail the sea surface. Physalia are distributed across the globe, and like many pelagic organisms, have been hypothesized to represent a massive, well-mixed population that extends across ocean basins. We tested this hypothesis by sequencing whole genomes of 133 samples collected from waters of over a dozen countries around the globe. Our results revealed five distinct lineages, with multiple lines of evidence indicating strong reproductive isolation, despite regions of range overlap. We combined these data with an independent dataset of thousands of images of Physalia uploaded to the citizen-science website inaturalist.org, which we scored for morphological characters including sail size, tentacle arrangement, and color. From these images, we identified four recognizable morphologies, described their geographical distribution, and linked them to four of the lineages identified with genomic data. We conclude there are at least four species, three of which correspond to species proposed by scientists in the 18th and 19th centuries: P. physalis, P utriculus, and P. megalista, along with one as yet unnamed species Physalia sp. from the Tasman Sea. Within each species, we observe significant population structure, with evidence of persistent subpopulations at a regional scale, as well as evidence for individual long-distance dispersal events. Our findings indicate that, instead of one well-mixed, cosmopolitan species, there are in fact multiple Physalia species with distinct but overlapping ranges, each made up of regionally endemic subpopulations that are connected by major ocean currents and wind patterns.

zoology↗

Comprehensive species sampling and sophisticated algorithmic approaches refute the monophyly of Arachnida

Deciphering the evolutionary relationships of Chelicerata (arachnids, horseshoe crabs, and allied taxa) has proven notoriously difficult, due to their ancient rapid radiation and the incidence of elevated evolutionary rates in several lineages. While conflicting hypotheses prevail in morphological and molecular datasets alike, the monophyly of Arachnida is nearly universally accepted. Though a small number of phylotranscriptomic analyses have recovered arachnid monophyly, these did not sample all living chelicerate orders. We generated a dataset of 506 high-quality genomes and transcriptomes, sampling all living orders of Chelicerata with high occupancy and rigorous approaches to orthology inference. Our analyses consistently recovered the nested placement of horseshoe crabs within a paraphyletic Arachnida. This result was insensitive to variation in evolutionary rates of genes, complexity of the substitution models, and alternatives algorithmic approaches to species tree inference. Investigation of systematic bias showed that genes and sites that recover arachnid monophyly are enriched in noise and exhibit low information content. To test the effect of morphological data, we generated a 514-taxon morphological data matrix of extant and fossil Chelicerata, analyzed in tandem with the molecular matrix. Combined analyses recovered the clade Merostomata (the marine orders Xiphosura, Eurypterida, and Chasmataspidida), but nested within Arachnida. Our results suggest that morphological convergence resulting from adaptations to life in terrestrial habitats has driven the historical perception of arachnid monophyly, paralleling the history of numerous other invertebrate terrestrial groups.

evolutionary biology↗

A phylogenomic framework for Vetigastropoda (Mollusca)

Abalones, turban snails, top snails, keyhole limpets and slit shells are just some of the diverse marine Vetigastropoda. With major lineages having ancient divergences in the Paleozoic Era, basal nodes in the phylogeny have been largely unresolved. Here we present the first genomic-scale dataset focused on vetigastropods, including a comprehensive sampling of taxa with all superfamilies and about half of the extant families (41 new transcriptomes, 49 total ingroup terminals). Our recovered topology is congruent among inference methods for the majority of nodes, and differs from previous studies, in which long branch attraction artifacts seem to be pervasive. The first three divergences sequentially separate Pleurotomarioidea, Seguenzioidea and Haliotoidea from remaining vetigastropods. Fissurelloidea is sister group to Scissurelloidea, Lepetodriloidea and Lepetelloidea, which all together are the sister group to Trochoidea. A methodological discordance exists in the position of Haliotidae and Fissurellidae, possibly due to a compounded effect of small sample bias derived from gene-wide partitioning. Dense sampling of trochoids and fissurellids also provides a backbone for family and subfamily-level relationships, with Tegulidae not monophyletic.

evolutionary biology↗

Deep gastropod relationships resolved

Gastropod mollusks are arguably the most diverse and abundant animals in the oceans, and are successful colonizers of terrestrial and freshwater environments. Here we resolve deep relationships between the five major gastropod lineages - Caenogastropoda, Heterobranchia, Neritimorpha, Patellogastropoda and Vetigastropoda - with highly congruent and supported phylogenomic analyses. We expand taxon sampling for underrepresented lineages with new transcriptomes, and conduct analyses accounting for the most pervasive sources of systematic errors in large datasets, namely compositional heterogeneity, site heterogeneity, heterotachy, variation in evolutionary rates among genes, matrix completeness and gene tree conflict. We find that vetigastropods and patellogastropods are sister taxa, and that neritimorphs are the sister group to caenogastropods and heterobranchs. With this topology, we reject the traditional Archaeogastropoda, which united neritimorphs, vetigastropods and patellogastropods, and is still used in the organization of collections of many natural history museums. Several traits related to development and life history support our molecular results. Importantly, the time of differentiation of the embryonic 4d cell (mesentoblast, responsible for mesoderm formation), differs between the two major clades, highlighting the degree of conservation and significance of development in the evolution of gastropods, as it is also known for spiralian animals more broadly.

evolutionary biology↗