Reconstruction of proto-vertebrate, proto-cyclostome and proto-gnathostome genomes provides new insights into early vertebrate evolution

Abstract

Ancient polyploidization events have had a lasting impact on vertebrate genome structure, organization and function. Some key questions regarding the number of ancient polyploidization events and their timing in relation to the cyclostome-gnathostome divergence have remained contentious. Here we generate de novo long-read-based chromosome-scale genome assemblies for the Japanese lamprey and elephant shark. Using these and other representative genomes and developing algorithms for the probabilistic macrosynteny model, we reconstruct high-resolution proto-vertebrate, proto-cyclostome and proto-gnathostome genomes. Our reconstructions resolve key questions regarding the early evolutionary history of vertebrates. First, cyclostomes diverged from the lineage leading to gnathostomes after a shared tetraploidization (1R) but before a gnathostome-specific tetraploidization (2R). Second, the cyclostome lineage experienced an additional hexaploidization. Third, 2R in the gnathostome lineage was an allotetraploidization event, and biased gene loss from one of the subgenomes shaped the gnathostome genome by giving rise to remarkably conserved microchromosomes. Thus, our reconstructions reveal the major evolutionary events and offer new insights into the origin and evolution of vertebrate genomes.

Whole-Genome Duplications and the Diversification of the Globin-X Genes of Vertebrates

“…The conserved synteny and phylogenetic analyses suggest that the PLEKHG3 and GbX genes of cyclostomes coduplicated, which would indicate that they derive from a segmental duplication or even a WGD. In this regard, our results are consistent with previous studies that indicate that lamprey genomes underwent an additional polyploidization by either a WGD ( Mehta et al 2013 ), hexaploidization via hybridization between tetraploid and diploid lineages ( Nakatani et al 2021 ), or extensive segmental duplications ( Smith and Keinath 2015 ).…”

“…There is less agreement about the placement of 2R on the vertebrate tree ( Kuraku et al 2009 ). The most recent studies place 2R in the last common ancestor of gnathostomes ( Simakov et al 2020 ; Nakatani et al 2021 ), and suggest that cyclostomes underwent an additional and independent polyploidization early in their evolution ( Mehta et al 2013 ; Nakatani et al 2021 ), whereas other authors place 2R in the common ancestor of cyclostomes and gnathostomes ( Sacerdot et al 2018 ). Under the first scenario, 1R would have given rise to the proto GbX gene of gnathostomes and the proto GbX-C gene of cyclostomes, followed by reciprocal losses of proto-GbX-C in the common ancestor of gnathostomes and of proto-GbX in the ancestor of cyclostomes ( fig.…”

“…WGDs, polyploidizations, and gene losses are mapped to their corresponding branch. We placed the 1R and 2R WGDs following Simakov et al (2020) and Nakatani et al (2021) . Symbols on a branch are arranged according to their relative order.…”

“…Asterisks on top of the vertical bars denote WGDs that gave rise to GbX paralogs present in extant species. The polyploidization event on the cyclostome branch could be an additional WGD ( Mehta et al 2013 ) or an hexaploidization due to hybridization between diploid and tetraploid lineages ( Nakatani et al 2021 ). Note that a full tree of all species examined would include 2 additional tandem duplications and multiple additional gene losses.…”

The Dopaminergic Control of Movement-Evolutionary Considerations

“…Thus, their ability to bind dopamine as a neurotransmitter is one of their few common features, and it has been proposed that this capacity was acquired by convergent evolution [ 17 , 18 ]. Several subtypes have been found within each family, and the repertoire of receptors varies depending on the vertebrate lineage ( Figure 1 c) as a result of whole genome duplications (WGDs) occurring in early vertebrate evolution [ 19 ], as well as lineage-specific gene losses. D 1A and D 1B are the only D 1 -like receptors present in mammals (also known as D 1 and D 5 in humans), whereas additional subtypes have been found in other vertebrates, namely, the D 1C and D 1D subtypes.…”