Ancient gene linkages support ctenophores as sister to other animals

[erik simpson]

This also posted in sci.bio.paleontology, and repeated here for general relevance to evolutionary interest.

Abstract

A central question in evolutionary biology is whether sponges or ctenophores (comb jellies) are the sister group to all other animals. These alternative phylogenetic hypotheses imply different scenarios for the evolution of complex neural systems and other animal-specific traits1,2,3,4,5,6. Conventional phylogenetic approaches based on morphological characters and increasingly extensive gene sequence collections have not been able to definitively answer this question7,8,9,10,11. Here we develop chromosome-scale gene linkage, also known as synteny, as a phylogenetic character for resolving this question12. We report new chromosome-scale genomes for a ctenophore and two marine sponges, and for three unicellular relatives of animals (a choanoflagellate, a filasterean amoeba and an ichthyosporean) that serve as outgroups for phylogenetic analysis. We find ancient syntenies that are conserved between animals and their close unicellular relatives. Ctenophores and unicellular eukaryotes share ancestral metazoan patterns, whereas sponges, bilaterians, and cnidarians share derived chromosomal rearrangements. Conserved syntenic characters unite sponges with bilaterians, cnidarians, and placozoans in a monophyletic clade to the exclusion of ctenophores, placing ctenophores as the sister group to all other animals. The patterns of synteny shared by sponges, bilaterians, and cnidarians are the result of rare and irreversible chromosome fusion-and-mixing events that provide robust and unambiguous phylogenetic support for the ctenophore-sister hypothesis. These findings provide a new framework for resolving deep, recalcitrant phylogenetic problems and have implications for our understanding of animal evolution.

https://www.nature.com/articles/s41586-023-05936-6 (open access)

[RonO]

This paper uses synteny (how the genes are grouped on the different
chromosomes). They claim that they can identify 14 syntenic groups of
genes that are on different chromosomes of single celled animals that
produce an evolutionary phylogeny consistent with Ctenophora branching
off from the lineage that became multicellular animals before Porifera
(sponges). Previous work had had Cnidaria and Bilateria being most
closely related to one lineage of sponge. They note that Ctenophora did
not consistently go with the other multicellular animals. Their
research supports Ctenophora branching off before sponges. This would
mean that Porifera may have lost some traits that the common ancestor of
the lineage of multicellular animals possessed.

It isn't just one shared change in synteny shared by Porifera and
Cnidaria and bilateral animals. The 14 syntenic groups found in single
celled animals found in Ctenophora have combined into 7 syntenic groups
in the other multicellular groups. This would have happened by
chromosome fusions or translocations. It is highly unlikely that the
syntenic groups were undone after the 14 were combined down to 7.
Sponges share the reduced syntenic grouping with Cnidaria and bilateral
animals, but Ctenophores retain them as 14 syntenic groups like single
celled animals.

So these researchers are not using DNA sequence differences to determine
the phylogeny, but macro changes to the genome in terms of what genes
are grouped with other genes on the chromosomes.

Ron Okimoto

[*Hemidactylus*]

Is that ctenable?

[RonO]

It seems to be the cnadir of the old phylogeny.

Something similar was done with the first mitochondrial genomes in order
to try to use the order of the genes in the mitochondrial genome to sort
out the star radiation pattern (pretty much reflecting the Cambrian
explosion). Some inversions and transpositions of genes within the
circular mitochondrial genome supported one of the phylogenies derived
from the sequence.

Ron Okimoto

[DB Cates]

I'd give it a cniddle.
--
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Don Cates ("he's a cunning rascal" PN)