Holosteans contextualize the role of the teleost genome duplication in promoting the rise of evolutionary novelties in the ray-finned fish innate immune system

Abstract

Over 99% of ray-finned fishes (Actinopterygii) are teleosts, a clade that comprises half of all living vertebrates that have diversified across virtually all fresh and saltwater ecosystems. This ecological diversity raises the question of how the immunogenetic diversity required to persist under heterogeneous pathogen pressures evolved. The teleost genome duplication (TGD) has been hypothesized as the evolutionary event that provided the genomic substrate for rapid genomic evolution and innovation. However, studies of putative teleost-specific innate immune receptors have been largely limited to comparisons either among teleosts or between teleosts and distantly related vertebrate clades such as tetrapods. Here we describe and characterize the receptor diversity of two clustered innate immune gene families in the teleost sister lineage: Holostei (bowfin and gars). Using genomic and transcriptomic data, we provide a detailed investigation of the phylogenetic history and conserved synteny of gene clusters encoding diverse immunoglobulin domain-containing proteins (DICPs) and novel immune-type receptors (NITRs). These data demonstrate an ancient linkage of DICPs to the major histocompatibility complex (MHC) and reveal an evolutionary origin of NITR variable-joining (VJ) exons that predate the TGD by at least 50 million years. Further characterizing the receptor diversity of Holostean DICPs and NITRs illuminates a sequence diversity that rivals the diversity of these innate immune receptor families in many teleosts. Taken together, our findings provide important historical context for the evolution of these gene families that challenge prevailing expectations concerning the consequences of the TGD during actinopterygiian evolution.

Phylogenomic analysis of the bowfin (Amia calva) reveals unrecognized species diversity in a living fossil lineage

“…These groups of fishes are generally characterized by lower species diversity, slower rates of molecular evolution in protein-coding genes and, in the case of species in the Infraclass Holostei (Bowfin and Gars), smaller genome sizes relative to teleosts 2 – 7 . In holosteans, these genomic characteristics have been attributed, at least in part, to their divergence prior to a whole-genome duplication (WGD) at the base of the teleost radiation, which has been hypothesized to have facilitated teleost diversification through the adaptive evolution of newly available paralogs of existing genes 4 , 6 , 8 – 10 , although differing viewpoints and caveats have begun to gain some support 11 – 14 . The same aspects of their genomes that have caused holostean fishes to become emerging model systems in studies of vertebrate genome evolution also, however, have the potential to complicate molecular phylogenetic examinations of these taxa, with multiple loci generally needed to fully resolve intra- and interspecific relationships 15 , 16 .…”

A chromosome-level genome assembly of longnose gar, Lepisosteus osseus

“…Holostean genomes have been demonstrated to be critical for understanding gene synteny and homology of complex genomic regions between teleosts and other vertebrates ( Braasch et al 2016 ; Bi et al 2021 ; Thompson et al 2021 ). Being the closest living relatives of teleosts, holosteans provide particularly informative context for understanding whether genomic novelties identified in teleosts are in fact unique to teleosts and for linking teleost and other vertebrate genomes ( Braasch et al 2016 ; Dornburg et al 2021 ; Thompson et al 2021 ; Dornburg and Yoder 2022 ).…”

Ancient Fish Lineages Illuminate Toll-Like Receptor Diversification in Early Vertebrate Evolution

“…While the evolution of this mode of immunity has had a tremendous effect on the coevolutionary arms race between vertebrate hosts and their pathogens (Nourmohammad et al 2016;Laanto et al 2017), the diversity of vertebrate innate immune receptors has historically received considerably less attention (Cunliffe 2006). A flurry of studies have cast new light on this neglected topic, revealing an immense scope of sequence and gene family diversity we are only beginning to understand (Langevin et al 2013;Dornburg et al 2021b;Dornburg and Yoder 2022), as well as surprising key interactions between innate and adaptive immune responses (Clemente et al 2016;Gianchecchi et al 2018). Further, the realization that innate immune responses can be trained has led to a call for fundamental change in our perspective of immunological memory (Netea et al 2019).…”