{"id":164103,"date":"2023-05-18T00:25:56","date_gmt":"2023-05-18T05:25:56","guid":{"rendered":"https:\/\/lifeboat.com\/blog\/2023\/05\/ancient-gene-linkages-support-ctenophores-as-sister-to-other-animals"},"modified":"2023-05-18T00:25:56","modified_gmt":"2023-05-18T05:25:56","slug":"ancient-gene-linkages-support-ctenophores-as-sister-to-other-animals","status":"publish","type":"post","link":"https:\/\/lifeboat.com\/blog\/2023\/05\/ancient-gene-linkages-support-ctenophores-as-sister-to-other-animals","title":{"rendered":"Ancient gene linkages support ctenophores as sister to other animals"},"content":{"rendered":"<p><a class=\"aligncenter blog-photo\" href=\"https:\/\/lifeboat.com\/blog.images\/ancient-gene-linkages-support-ctenophores-as-sister-to-other-animals.jpg\"><\/a><\/p>\n<p>As sponges and ctenophores are such disparate animals<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 13\" title=\"Dunn, C. W., Leys, S. P. & Haddock, S. H. D. The hidden biology of sponges and ctenophores. Trends Ecol. Evol. 30282&ndash;291 (2015).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR13\" id=\"ref-link-section-d40933302e628\">13<\/a><\/sup>, the nature of the first diverging animal lineage has implications for the evolution of fundamental animal characteristics. Adult sponges are generally sessile filter-feeding organisms with body plans organized into reticulated water-filtration channels, structures built out of silica or calcium carbonate, and specialized cell types and tissues used for feeding, reproduction and self-defence, but they lack neuronal and muscle cells<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 15\" title=\"Musser, J. M. et al. Profiling cellular diversity in sponges informs animal cell type and nervous system evolution. Science 374717&ndash;723 (2021).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR15\" id=\"ref-link-section-d40933302e632\">15<\/a><\/sup>. By contrast, ctenophores are gelatinous marine predators that move using eight longitudinal \u2018comb rows\u2019 of ciliary bundles<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 16\" title=\"Harbison, G. R. in The Origins and Relationships of Lower Invertebrates Systematics Association Special Vol. 28 (eds Morris, S. C. et al.) 78&ndash;100 (Clarendon Press, 1985).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR16\" id=\"ref-link-section-d40933302e636\">16<\/a>,<a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 17\" title=\"Tamm, S. L. Formation of the statolith in the ctenophore Mnemiopsis leidyi. Biol. Bull. 227, 7&ndash;18 (2014).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR17\" id=\"ref-link-section-d40933302e639\">17<\/a><\/sup>; they are superficially similar but unrelated to cnidarian medusae<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 13\" title=\"Dunn, C. W., Leys, S. P. & Haddock, S. H. D. The hidden biology of sponges and ctenophores. Trends Ecol. Evol. 30282&ndash;291 (2015).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR13\" id=\"ref-link-section-d40933302e643\">13<\/a>,<a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 18\" title=\"Burton, P. M. Insights from diploblasts; the evolution of mesoderm and muscle. J. Exp. Zool. B 310, 5&ndash;14 (2008).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR18\" id=\"ref-link-section-d40933302e646\">18<\/a><\/sup> and possess multiple nerve nets<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 19\" title=\"Sachkova, M. Y. et al. Neuropeptide repertoire and 3D anatomy of the ctenophore nervous system. Curr. Biol. 31, 5274&ndash;5285 (2021).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR19\" id=\"ref-link-section-d40933302e650\">19<\/a><\/sup>. Thus, whereas the sponge-sister scenario suggests a single origin of neurons on the ctenophore\u2013parahoxozoan stem, the ctenophore-sister scenario implies either that either ancestral metazoan neurons were lost in the sponge lineage, or that there was convergent evolution of neurons in the ctenophore and parahoxozoan lineages<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 3\" title=\"J\u00e9kely, G., Paps, J. & Nielsen, C. The phylogenetic position of ctenophores and the origin(s) of nervous systems. Evodevo 6, 1 (2015).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR3\" id=\"ref-link-section-d40933302e655\">3<\/a>,<a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 6\" title=\"Burkhardt, P. Ctenophores and the evolutionary origin(s) of neurons. Trends Neurosci. 45878&ndash;880 (2022).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR6\" id=\"ref-link-section-d40933302e658\">6<\/a><\/sup>. Similar considerations apply to other metazoan cell types<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 18\" title=\"Burton, P. M. Insights from diploblasts; the evolution of mesoderm and muscle. J. Exp. Zool. B 310, 5&ndash;14 (2008).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR18\" id=\"ref-link-section-d40933302e662\">18<\/a><\/sup>, gene regulatory networks, animal development<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 13\" title=\"Dunn, C. W., Leys, S. P. & Haddock, S. H. D. The hidden biology of sponges and ctenophores. Trends Ecol. Evol. 30282&ndash;291 (2015).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR13\" id=\"ref-link-section-d40933302e666\">13<\/a>,<a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 18\" title=\"Burton, P. M. Insights from diploblasts; the evolution of mesoderm and muscle. J. Exp. Zool. B 310, 5&ndash;14 (2008).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR18\" id=\"ref-link-section-d40933302e669\">18<\/a><\/sup> and other uniquely metazoan features.<\/p>\n<p>Despite its importance for understanding animal evolution, the relative branching order of sponges, ctenophores and other animals has proven to be difficult to resolve<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 2\" title=\"Halanych, K. M. The ctenophore lineage is older than sponges? That cannot be right! Or can it? J. Exp. Biol. 218592&ndash;597 (2015).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR2\" id=\"ref-link-section-d40933302e676\">2<\/a><\/sup>. The fossil record is largely silent on this issue as verified Precambrian sponge fossils are extremely rare<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 20\" title=\"Antcliffe, J. B., Callow, R. H. T. & Brasier, M. D. Giving the early fossil record of sponges a squeeze. Biol. Rev. Camb. Philos. Soc. 89972&ndash;1004 (2014).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR20\" id=\"ref-link-section-d40933302e680\">20<\/a><\/sup> and putative fossils of the soft-bodied ctenophores are difficult to interpret<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 21\" title=\"O\u2019Brien, L. J. & Caron, J.-B. A new stalked filter-feeder from the middle Cambrian Burgess Shale, British Columbia, Canada. PLoS ONE 7, e29233 (2012).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR21\" id=\"ref-link-section-d40933302e684\">21<\/a><\/sup>. Morphological characters of living groups (for example, choanocytes of sponges) are not sufficient to resolve the question because true homology is difficult to assign, and such characters are easily lost or can arise convergently<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 13\" title=\"Dunn, C. W., Leys, S. P. & Haddock, S. H. D. The hidden biology of sponges and ctenophores. Trends Ecol. Evol. 30282&ndash;291 (2015).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR13\" id=\"ref-link-section-d40933302e688\">13<\/a>,<a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 22\" title=\"Mah, J. L. & Leys, S. P. Think like a sponge: the genetic signal of sensory cells in sponges. Dev. Biol. 431, 93&ndash;100 (2017).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR22\" id=\"ref-link-section-d40933302e691\">22<\/a><\/sup>. The ctenophore-sister hypothesis is supported by a pair of gene duplications shared by sponges, bilaterians, placozoans and cnidarians but not ctenophores<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 23\" title=\"Erives, A. & Fritzsch, B. A screen for gene paralogies delineating evolutionary branching order of early metazoa. G3 10811&ndash;826 (2020).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR23\" id=\"ref-link-section-d40933302e695\">23<\/a><\/sup>. Although sophisticated methods for sequence-based phylogenomics have been developed and applied to increasingly large molecular datasets, there is still considerable debate about the relative position of sponges and ctenophores as results are sensitive to how sequence evolution is modelled<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 11\" title=\"Li, Y., Shen, X.-X., Evans, B., Dunn, C. W. & Rokas, A. Rooting the animal tree of life. Mol. Biol. Evol. 38, 4322&ndash;4333 (2021).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR11\" id=\"ref-link-section-d40933302e700\">11<\/a><\/sup>, which taxa or sites are included<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 24\" title=\"Shen, X.-X., Hittinger, C. T., Rokas, A., Minh, B. Q. & Braun, E. L. Contentious relationships in phylogenomic studies can be driven by a handful of genes. Nat. Ecol. Evol. 1, 0126 (2017).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR24\" id=\"ref-link-section-d40933302e704\">24<\/a>,<a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 25\" title=\"Francis, W. R. & Canfield, D. E. Very few sites can reshape the inferred phylogenetic tree. PeerJ 8, e8865 (2020).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR25\" id=\"ref-link-section-d40933302e707\">25<\/a><\/sup>, and the effects of long-branch artifacts and nucleotide compositional variation<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 26\" title=\"Kapli, P., Yang, Z. & Telford, M. J. Phylogenetic tree building in the genomic age. Nat. Rev. Genet. 21428&ndash;444 (2020).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR26\" id=\"ref-link-section-d40933302e711\">26<\/a><\/sup>. New approaches are needed.<\/p>\n<p>We reasoned that patterns of synteny, classically defined as chromosomal gene linkage without regard to gene order<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 27\" title=\"Renwick, J. H. The mapping of human chromosomes. Annu. Rev. Genet. 5, 81&ndash;120 (1971).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR27\" id=\"ref-link-section-d40933302e718\">27<\/a><\/sup>, could provide a powerful tool for resolving the ctenophore-sister versus sponge-sister debate. Chromosomal patterns of gene linkage evolve slowly in many lineages<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 12\" title=\"Simakov, O. et al. Deeply conserved synteny and the evolution of metazoan chromosomes. Sci. Adv. 8, eabi5884 (2022).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR12\" id=\"ref-link-section-d40933302e722\">12<\/a>,<a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" title=\"Muller, H. J. in The New Systematics (ed. Huxley, J.) 185&ndash;268 (Oxford Univ. Press, 1940).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR28\" id=\"ref-link-section-d40933302e725\">28<\/a>,<a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" title=\"Drosophila 12 Genomes Consortium. Evolution of genes and genomes on the Drosophila phylogeny. Nature 450203&ndash;218 (2007).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR29\" id=\"ref-link-section-d40933302e725_1\">29<\/a>,<a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 30\" title=\"Hane, J. K. et al. A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biol. 12, R45 (2011).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR30\" id=\"ref-link-section-d40933302e728\">30<\/a><\/sup>, probably because it is improbable for interchromosomal translocations to be fixed in populations with large effective population sizes<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 28\" title=\"Muller, H. J. in The New Systematics (ed. Huxley, J.) 185&ndash;268 (Oxford Univ. Press, 1940).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR28\" id=\"ref-link-section-d40933302e732\">28<\/a>,<a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 31\" title=\"Wright, S. On the probability of fixation of reciprocal translocations. Am. Nat. 75513&ndash;522 (1941).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR31\" id=\"ref-link-section-d40933302e735\">31<\/a>,<a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 32\" title=\"Lv, J., Havlak, P. & Putnam, N. H. Constraints on genes shape long-term conservation of macro-synteny in metazoan genomes. BMC Bioinform. 12, S11 (2011).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR32\" id=\"ref-link-section-d40933302e738\">32<\/a><\/sup>. Notably, some changes in synteny are effectively irreversible. For example, when two distinct ancestral synteny groups are combined onto a single chromosome by translocation, and subsequent intrachromosomal rearrangements mix these two groups of genes, it is very unlikely that the ancestral separated pattern will be restored by further rearrangement and fission, in the same sense that spontaneous reduction in entropy is improbable<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 12\" title=\"Simakov, O. et al. Deeply conserved synteny and the evolution of metazoan chromosomes. Sci. Adv. 8, eabi5884 (2022).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR12\" id=\"ref-link-section-d40933302e742\">12<\/a><\/sup>. Such rare and irreversible changes are particularly useful for resolving challenging phylogenetic questions as they give rise to shared derived features that unambiguously unite all descendant lineages<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" title=\"Hillis, D. M. SINEs of the perfect character. Proc. Natl Acad. Sci. USA 96, 9979&ndash;9981 (1999).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR33\" id=\"ref-link-section-d40933302e746\">33<\/a>,<a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" title=\"Rokas, A. & Holland, P. W. Rare genomic changes as a tool for phylogenetics. Trends Ecol. Evol. 15454&ndash;459 (2000).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR34\" id=\"ref-link-section-d40933302e746_1\">34<\/a>,<a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 35\" title=\"Okada, N. SINEs: Short interspersed repeated elements of the eukaryotic genome. Trends Ecol. Evol. 6358&ndash;361 (1991).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR35\" id=\"ref-link-section-d40933302e749\">35<\/a><\/sup>. Deeply conserved syntenies observed between animals and their closest unicellular relatives<sup><a data-track=\"click\" data-track-action=\"reference anchor\" data-track-label=\"link\" data-test=\"citation-ref\" aria-label=\"Reference 12\" title=\"Simakov, O. et al. Deeply conserved synteny and the evolution of metazoan chromosomes. Sci. Adv. 8, eabi5884 (2022).\" href=\"https:\/\/www.nature.com\/articles\/s41586-023-05936-6#ref-CR12\" id=\"ref-link-section-d40933302e754\">12<\/a><\/sup> suggest that outgroup comparisons could be used to infer ancestral metazoan states and polarize changes within animals to address the sponge-sister versus ctenophore-sister debate. Yet, chromosome-scale genome sequences of the unicellular or colonial eukaryotic outgroups closest to animals (choanoflagellates, filastereans and ichthyosporeans) have not been reported.<\/p>\n","protected":false},"excerpt":{"rendered":"<p>As sponges and ctenophores are such disparate animals13, the nature of the first diverging animal lineage has implications for the evolution of fundamental animal characteristics. Adult sponges are generally sessile filter-feeding organisms with body plans organized into reticulated water-filtration channels, structures built out of silica or calcium carbonate, and specialized cell types and tissues used [\u2026]<\/p>\n","protected":false},"author":662,"featured_media":0,"comment_status":"open","ping_status":"closed","sticky":false,"template":"","format":"standard","meta":{"footnotes":""},"categories":[11,385,412,47],"tags":[],"class_list":["post-164103","post","type-post","status-publish","format-standard","hentry","category-biotech-medical","category-evolution","category-genetics","category-neuroscience"],"_links":{"self":[{"href":"https:\/\/lifeboat.com\/blog\/wp-json\/wp\/v2\/posts\/164103","targetHints":{"allow":["GET"]}}],"collection":[{"href":"https:\/\/lifeboat.com\/blog\/wp-json\/wp\/v2\/posts"}],"about":[{"href":"https:\/\/lifeboat.com\/blog\/wp-json\/wp\/v2\/types\/post"}],"author":[{"embeddable":true,"href":"https:\/\/lifeboat.com\/blog\/wp-json\/wp\/v2\/users\/662"}],"replies":[{"embeddable":true,"href":"https:\/\/lifeboat.com\/blog\/wp-json\/wp\/v2\/comments?post=164103"}],"version-history":[{"count":0,"href":"https:\/\/lifeboat.com\/blog\/wp-json\/wp\/v2\/posts\/164103\/revisions"}],"wp:attachment":[{"href":"https:\/\/lifeboat.com\/blog\/wp-json\/wp\/v2\/media?parent=164103"}],"wp:term":[{"taxonomy":"category","embeddable":true,"href":"https:\/\/lifeboat.com\/blog\/wp-json\/wp\/v2\/categories?post=164103"},{"taxonomy":"post_tag","embeddable":true,"href":"https:\/\/lifeboat.com\/blog\/wp-json\/wp\/v2\/tags?post=164103"}],"curies":[{"name":"wp","href":"https:\/\/api.w.org\/{rel}","templated":true}]}}