Publications by authors named "Jesus Lozano-Fernandez"

11 Publications

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Arachnid monophyly: Morphological, palaeontological and molecular support for a single terrestrialization within Chelicerata.

Arthropod Struct Dev 2020 Nov 9;59:100997. Epub 2020 Oct 9.

Institute of Evolutionary Biology (CSIC-UPF), Barcelona, Spain; School of Biological Sciences, University of Bristol, Bristol, UK. Electronic address:

The majority of extant arachnids are terrestrial, but other chelicerates are generally aquatic, including horseshoe crabs, sea spiders, and the extinct eurypterids. It is necessary to determine whether arachnids are exclusively descended from a single common ancestor (monophyly), because only that relationship is compatible with one land colonisation in chelicerate evolutionary history. Some studies have cast doubt on arachnid monophyly and recast the origins of their terrestrialization. These include some phylogenomic analyses placing horseshoe crabs within Arachnida, and from aquatic Palaeozoic stem-group scorpions. Here, we evaluate the possibility of arachnid monophyly by considering morphology, fossils and molecules holistically. We argue arachnid monophyly obviates the need to posit reacquisition/retention of aquatic characters such as gnathobasic feeding and book gills without trabeculae from terrestrial ancestors in horseshoe crabs, and that the scorpion total-group contains few aquatic taxa. We built a matrix composed of 200 slowly-evolving genes and re-analysed two published molecular datasets. We retrieved arachnid monophyly where other studies did not - highlighting the difficulty of resolving chelicerate relationships from current molecular data. As such, we consider arachnid monophyly the best-supported hypothesis. Finally, we inferred that arachnids terrestrialized during the Cambrian-Ordovician using the slow-evolving molecular matrix, in agreement with recent analyses.
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http://dx.doi.org/10.1016/j.asd.2020.100997DOI Listing
November 2020

A Cambrian-Ordovician Terrestrialization of Arachnids.

Front Genet 2020 11;11:182. Epub 2020 Mar 11.

School of Biological Sciences, University of Bristol, Bristol, United Kingdom.

Understanding the temporal context of terrestrialization in chelicerates depends on whether terrestrial groups, the traditional Arachnida, have a single origin and whether or not horseshoe crabs are primitively or secondarily marine. Molecular dating on a phylogenomic tree that recovers arachnid monophyly, constrained by 27 rigorously vetted fossil calibrations, estimates that Arachnida originated during the Cambrian or Ordovician. After the common ancestor colonized the land, the main lineages appear to have rapidly radiated in the Cambrian-Ordovician boundary interval, coinciding with high rates of molecular evolution. The highest rates of arachnid diversification are detected between the Permian and Early Cretaceous. A pattern of ancient divergence estimates for terrestrial arthropod groups in the Cambrian while the oldest fossils are Silurian (seen in both myriapods and arachnids) is mirrored in the molecular and fossil records of land plants. We suggest the discrepancy between molecular and fossil evidence for terrestrialization is likely driven by the extreme sparseness of terrestrial sediments in the rock record before the late Silurian.
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http://dx.doi.org/10.3389/fgene.2020.00182DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7078165PMC
March 2020

Author Correction: Increasing species sampling in chelicerate genomic-scale datasets provides support for monophyly of Acari and Arachnida.

Nat Commun 2019 Oct 1;10(1):4534. Epub 2019 Oct 1.

University of Bristol School of Biological Sciences, 24 Tyndall Avenue, Bristol, BS8 1TQ, UK.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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http://dx.doi.org/10.1038/s41467-019-12259-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6773737PMC
October 2019

Pancrustacean Evolution Illuminated by Taxon-Rich Genomic-Scale Data Sets with an Expanded Remipede Sampling.

Genome Biol Evol 2019 08;11(8):2055-2070

Natural History Museum of Denmark, University of Copenhagen, Denmark.

The relationships of crustaceans and hexapods (Pancrustacea) have been much discussed and partially elucidated following the emergence of phylogenomic data sets. However, major uncertainties still remain regarding the position of iconic taxa such as Branchiopoda, Copepoda, Remipedia, and Cephalocarida, and the sister group relationship of hexapods. We assembled the most taxon-rich phylogenomic pancrustacean data set to date and analyzed it using a variety of methodological approaches. We prioritized low levels of missing data and found that some clades were consistently recovered independently of the analytical approach used. These include, for example, Oligostraca and Altocrustacea. Substantial support was also found for Allotriocarida, with Remipedia as the sister of Hexapoda (i.e., Labiocarida), and Branchiopoda as the sister of Labiocarida, a clade that we name Athalassocarida (="nonmarine shrimps"). Within Allotriocarida, Cephalocarida was found as the sister of Athalassocarida. Finally, moderate support was found for Hexanauplia (Copepoda as sister to Thecostraca) in alliance with Malacostraca. Mapping key crustacean tagmosis patterns and developmental characters across the revised phylogeny suggests that the ancestral pancrustacean was relatively short-bodied, with extreme body elongation and anamorphic development emerging later in pancrustacean evolution.
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http://dx.doi.org/10.1093/gbe/evz097DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6684935PMC
August 2019

Increasing species sampling in chelicerate genomic-scale datasets provides support for monophyly of Acari and Arachnida.

Nat Commun 2019 05 24;10(1):2295. Epub 2019 May 24.

University of Bristol School of Biological Sciences, 24 Tyndall Avenue, Bristol, BS8 1TQ, UK.

Chelicerates are a diverse group of arthropods, represented by such forms as predatory spiders and scorpions, parasitic ticks, humic detritivores, and marine sea spiders (pycnogonids) and horseshoe crabs. Conflicting phylogenetic relationships have been proposed for chelicerates based on both morphological and molecular data, the latter usually not recovering arachnids as a clade and instead finding horseshoe crabs nested inside terrestrial Arachnida. Here, using genomic-scale datasets and analyses optimised for countering systematic error, we find strong support for monophyletic Acari (ticks and mites), which when considered as a single group represent the most biodiverse chelicerate lineage. In addition, our analysis recovers marine forms (sea spiders and horseshoe crabs) as the successive sister groups of a monophyletic lineage of terrestrial arachnids, suggesting a single colonisation of land within Chelicerata and the absence of wholly secondarily marine arachnid orders.
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http://dx.doi.org/10.1038/s41467-019-10244-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6534568PMC
May 2019

Homeobox Gene Duplication and Divergence in Arachnids.

Mol Biol Evol 2018 09;35(9):2240-2253

Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, United Kingdom.

Homeobox genes are key toolkit genes that regulate the development of metazoans and changes in their regulation and copy number have contributed to the evolution of phenotypic diversity. We recently identified a whole genome duplication (WGD) event that occurred in an ancestor of spiders and scorpions (Arachnopulmonata), and that many homeobox genes, including two Hox clusters, appear to have been retained in arachnopulmonates. To better understand the consequences of this ancient WGD and the evolution of arachnid homeobox genes, we have characterized and compared the homeobox repertoires in a range of arachnids. We found that many families and clusters of these genes are duplicated in all studied arachnopulmonates (Parasteatoda tepidariorum, Pholcus phalangioides, Centruroides sculpturatus, and Mesobuthus martensii) compared with nonarachnopulmonate arachnids (Phalangium opilio, Neobisium carcinoides, Hesperochernes sp., and Ixodes scapularis). To assess divergence in the roles of homeobox ohnologs, we analyzed the expression of P. tepidariorum homeobox genes during embryogenesis and found pervasive changes in the level and timing of their expression. Furthermore, we compared the spatial expression of a subset of P. tepidariorum ohnologs with their single copy orthologs in P. opilio embryos. We found evidence for likely subfunctionlization and neofunctionalization of these genes in the spider. Overall our results show a high level of retention of homeobox genes in spiders and scorpions post-WGD, which is likely to have made a major contribution to their developmental evolution and diversification through pervasive subfunctionlization and neofunctionalization, and paralleling the outcomes of WGD in vertebrates.
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http://dx.doi.org/10.1093/molbev/msy125DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6107062PMC
September 2018

Soft-Bodied Fossils Are Not Simply Rotten Carcasses - Toward a Holistic Understanding of Exceptional Fossil Preservation: Exceptional Fossil Preservation Is Complex and Involves the Interplay of Numerous Biological and Geological Processes.

Bioessays 2018 Jan 29;40(1). Epub 2017 Nov 29.

School of Earth Sciences, University of Bristol, Wills Memorial Building, Queen's Road, Bristol, BS8 1RJ, UK.

Exceptionally preserved fossils are the product of complex interplays of biological and geological processes including burial, autolysis and microbial decay, authigenic mineralization, diagenesis, metamorphism, and finally weathering and exhumation. Determining which tissues are preserved and how biases affect their preservation pathways is important for interpreting fossils in phylogenetic, ecological, and evolutionary frameworks. Although laboratory decay experiments reveal important aspects of fossilization, applying the results directly to the interpretation of exceptionally preserved fossils may overlook the impact of other key processes that remove or preserve morphological information. Investigations of fossils preserving non-biomineralized tissues suggest that certain structures that are decay resistant (e.g., the notochord) are rarely preserved (even where carbonaceous components survive), and decay-prone structures (e.g., nervous systems) can fossilize, albeit rarely. As we review here, decay resistance is an imperfect indicator of fossilization potential, and a suite of biological and geological processes account for the features preserved in exceptional fossils.
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http://dx.doi.org/10.1002/bies.201700167DOI Listing
January 2018

RelTime Rates Collapse to a Strict Clock When Estimating the Timeline of Animal Diversification.

Genome Biol Evol 2017 05;9(5):1320-1328

School of Earth Sciences, Life Sciences Building, University of Bristol, United Kingdom.

Establishing an accurate timescale for the history of life is crucial to understand evolutionary processes. For this purpose, relaxed molecular clock models implemented in a Bayesian MCMC framework are generally used. However, these methods are time consuming. RelTime, a non-Bayesian method implementing a fast, ad hoc, algorithm for relative dating, was developed to overcome the computational inefficiencies of Bayesian software. RelTime was recently used to investigate the timing of origin of animals, yielding results consistent with early strict clock studies from the 1980s and 1990s, estimating metazoans to have a Mesoproterozoic origin-over a billion years ago. RelTime results are unexpected and disagree with the largest majority of modern, relaxed, Bayesian molecular clock analyses, which suggest animals originated in the Tonian-Cryogenian (less that 850 million years ago). Here, we demonstrate that RelTime-inferred divergence times for the origin of animals are spurious, a consequence of the inability of RelTime to relax the clock along the internal branches of the animal phylogeny. RelTime-inferred divergence times are comparable to strict-clock estimates because they are essentially inferred under a strict clock. Our results warn us of the danger of using ad hoc algorithms making implicit assumptions about rate changes along a tree. Our study roundly rejects a Mesoproterozoic origin of animals; metazoans emerged in the Tonian-Cryogenian, and diversified in the Ediacaran, in the immediate prelude to the routine fossilization of animals in the Cambrian associated with the emergence of readily preserved skeletons.
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http://dx.doi.org/10.1093/gbe/evx079DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5447329PMC
May 2017

Uncertain-tree: discriminating among competing approaches to the phylogenetic analysis of phenotype data.

Proc Biol Sci 2017 01;284(1846)

School of Earth Sciences, University of Bristol, Life Sciences Building, 24 Tyndall Avenue, Bristol BS8 1TQ, UK

Morphological data provide the only means of classifying the majority of life's history, but the choice between competing phylogenetic methods for the analysis of morphology is unclear. Traditionally, parsimony methods have been favoured but recent studies have shown that these approaches are less accurate than the Bayesian implementation of the Mk model. Here we expand on these findings in several ways: we assess the impact of tree shape and maximum-likelihood estimation using the Mk model, as well as analysing data composed of both binary and multistate characters. We find that all methods struggle to correctly resolve deep clades within asymmetric trees, and when analysing small character matrices. The Bayesian Mk model is the most accurate method for estimating topology, but with lower resolution than other methods. Equal weights parsimony is more accurate than implied weights parsimony, and maximum-likelihood estimation using the Mk model is the least accurate method. We conclude that the Bayesian implementation of the Mk model should be the default method for phylogenetic estimation from phenotype datasets, and we explore the implications of our simulations in reanalysing several empirical morphological character matrices. A consequence of our finding is that high levels of resolution or the ability to classify species or groups with much confidence should not be expected when using small datasets. It is now necessary to depart from the traditional parsimony paradigms of constructing character matrices, towards datasets constructed explicitly for Bayesian methods.
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http://dx.doi.org/10.1098/rspb.2016.2290DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5247500PMC
January 2017

A molecular palaeobiological exploration of arthropod terrestrialization.

Philos Trans R Soc Lond B Biol Sci 2016 07;371(1699)

School of Earth Sciences, University of Bristol, Life Sciences Building, 24 Tyndall Avenue, Bristol BS8 1TQ, UK School of Biological Sciences, University of Bristol, Life Sciences Building, 24 Tyndall Avenue, Bristol BS8 1TQ, UK

Understanding animal terrestrialization, the process through which animals colonized the land, is crucial to clarify extant biodiversity and biological adaptation. Arthropoda (insects, spiders, centipedes and their allies) represent the largest majority of terrestrial biodiversity. Here we implemented a molecular palaeobiological approach, merging molecular and fossil evidence, to elucidate the deepest history of the terrestrial arthropods. We focused on the three independent, Palaeozoic arthropod terrestrialization events (those of Myriapoda, Hexapoda and Arachnida) and showed that a marine route to the colonization of land is the most likely scenario. Molecular clock analyses confirmed an origin for the three terrestrial lineages bracketed between the Cambrian and the Silurian. While molecular divergence times for Arachnida are consistent with the fossil record, Myriapoda are inferred to have colonized land earlier, substantially predating trace or body fossil evidence. An estimated origin of myriapods by the Early Cambrian precedes the appearance of embryophytes and perhaps even terrestrial fungi, raising the possibility that terrestrialization had independent origins in crown-group myriapod lineages, consistent with morphological arguments for convergence in tracheal systems.This article is part of the themed issue 'Dating species divergences using rocks and clocks'.
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http://dx.doi.org/10.1098/rstb.2015.0133DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4920334PMC
July 2016