Improved Understanding of the Role of Gene and Genome Duplications in Chordate Evolution With New Genome and Transcriptome Sequences

Abstract

Comparative approaches to understanding chordate genomes have uncovered a significant role for gene duplications, including whole genome duplications (WGDs), giving rise to and expanding gene families. In developmental biology, gene families created and expanded by both tandem and WGDs are paramount. These genes, often involved in transcription and signalling, are candidates for underpinning major evolutionary transitions because they are particularly prone to retention and subfunctionalisation, neofunctionalisation, or specialisation following duplication. Under the subfunctionalisation model, duplication lays the foundation for the diversification of paralogues, especially in the context of gene regulation. Tandemly duplicated paralogues reside in the same regulatory environment, which may constrain them and result in a gene cluster with closely linked but subtly different expression patterns and functions. Ohnologues (WGD paralogues) often diversify by partitioning their expression domains between retained paralogues, amidst the many changes in the genome during rediploidisation, including chromosomal rearrangements and extensive gene losses. The patterns of these retentions and losses are still not fully understood, nor is the full extent of the impact of gene duplication on chordate evolution. The growing number of sequencing projects, genomic resources, transcriptomics, and improvements to genome assemblies for diverse chordates from non-model and under-sampled lineages like the coelacanth, as well as key lineages, such as amphioxus and lamprey, has allowed more informative comparisons within developmental gene families as well as revealing the extent of conserved synteny across whole genomes. This influx of data provides the tools necessary for phylogenetically informed comparative genomics, which will bring us closer to understanding the evolution of chordate body plan diversity and the changes underpinning the origin and diversification of vertebrates.

Evolutionary diversification of the canonical Wnt signaling effector TCF/LEF in chordates

“…In the case of the synteny data, this mixture of different gnathostome‐like neighborhoods is consistent with something akin to the hypothesis of tetralogy (Aase‐Remedios & Ferrier, 2021 ; Martin & Holland, 2014 ), which would imply that the divergence of the cyclostome and gnathostome lineages occurred in a brief time period close to the 2R WGD events, such that there has been differential sorting of paralogs between cyclostomes versus gnathostomes during the process of rediploidization after the polyploidization events associated with the WGD. The mixed features present in the TCF/LEF genes themselves, when comparing cyclostomes versus gnathostomes, could then be accounted for by lineage‐specific ohnolog resolution (LORe) (Robertson et al., 2017 ), which was described for the salmonid WGD, but more generally describes the way that ohnologs that arise relatively close to the WGD events then experience independent divergence in the sister lineages arising close to the WGD.…”

“…The mixture of characteristics and their affinities in the cyclostome TCF genes relative to those of gnathostomes is consistent with their distribution during evolution via tetralogy and LORe (Aase‐Remedios & Ferrier, 2021 ; Martin & Holland, 2014 ; Robertson et al., 2017 ). Consequently, it seems reasonable to conclude that the ancestral pre‐WGD TCF gene of vertebrates (i.e., gnathostomes plus cyclostomes) would have been a composite of features found across the gnathostome TCF7 , LEF , TCF7L1 , and TCF7L2 ohnolog subfamilies as well as the cyclostome genes.…”

“…Our phylogenetic analysis also provides greater detail to more robustly support the hypothesis that the four gnathostome TCF/LEF subfamilies originated from the 2R WGD that occurred early in vertebrate evolution (Aase‐Remedios & Ferrier, 2021 ; Holland & Ocampo Daza, 2018 ). The topology of the phylogeny is consistent with the 1R WGD producing the two ohnologs that were the ancestors of the TCF7/LEF1 genes on the one hand and the TCF7L1/TCF7L2 genes on the other, followed by the second of the 2R WGD then producing the four gnathostome TCF/LEF ohnolog subfamilies: TCF7 , LEF1 , TCF7L1 , and TCF7L2 (Figure S2 ).…”

“…Due to the presence of four TCF/LEF genes in the genome of vertebrates, it has been assumed that these originated from a single TCF gene ancestor through the two rounds of whole‐genome duplications (2R WGD) that occurred at the base of vertebrate evolution (Aase‐Remedios & Ferrier, 2021 ; Holland & Ocampo Daza, 2018 ; Lamb, 2021 ). However, this hypothesis is currently based only on phylogenetic analyses that include a limited number of gnathostome species (Klingel et al., 2012 ; Zhu et al., 2021 ).…”

Early effects of gene duplication on the robustness and phenotypic variability of gene regulatory networks

“…Later evolution can then improve further such functions by adjusting one of the duplicate genes [ 12 , 13 ]. The debate on the preponderance of the different scenarios is lively and enriched by insightful theoretical studies and substantial empirical evidence [ 8 – 11 , 14 , 15 ].…”