Ancestral Physical Stress and Later Immune Gene Family Expansions Shaped Bivalve Mollusc Evolution

Abstract

Bivalve molluscs comprise 20,000 species occupying a wide diversity of marine habitats. As filter feeders and detritivores they act as ecosystem engineers clarifying water, creating reefs and protecting coastlines. The global decline of natural oyster reefs has led to increased restoration efforts in recent years. Bivalves also play an important role in global food security contributing to > 20% of worldwide aquaculture production. Despite this importance, relatively little is known about bivalve evolutionary adaptation strategies. Difficulties previously associated with highly heterozygous and repetitive regions of bivalve genomes have been overcome by long read sequencing, enabling the generation of accurate bivalve assemblies. With these resources we have analysed the genomes of 32 species representing each molluscan class, including 15 bivalve species, to identify gene families that have undergone expansion during bivalve evolution. Gene family expansions across bivalve genomes occur at the point of evolutionary pressures. We uncovered two key factors that shape bivalve evolutionary history: expansion of bivalvia into environmental niches with high stress followed by later exposure to specific pathogenic pressures. The conserved expansion of protein recycling gene families we found across bivalvia is mirrored by adaptations to a sedentary lifestyle seen in plants. These results reflect the ability of bivalves to tolerate high levels of environmental stress and constant exposure to pathogens as filter feeders. The increasing availability of accurate genome assemblies will provide greater resolution to these analyses allowing further points of evolutionary pressure to become clear in other understudied taxa and potentially different populations of a single species.

Chromosome level reference genome for European flat oyster (Ostrea edulis L.)

“…We inferred gene family expansions in O. edulis building on a published strategy (Regan et al, 2021). The start-point was all predicted proteins from the genome assemblies of 16 bivalve species, inclusive of OE_Roslin_V1 (Supplementary Table 1).…”

“…FastTree (Price et al, 2010) was used to infer gene trees per orthogroup, which were compared against the rooted species tree by Orthofinder to infer duplications/losses using a duplication-loss-coalescent model (Emms & Kelly, 2019). Kinfin v1.0 (Laetsch & Blaxter, 2017a) was used to identify orthogroups that showed evidence for gene expansion in O. edulis compared to other bivalves (Regan et al,. 2021).…”

“…We inferred gene family expansions in O. edulis building on a published strategy (Regan et al, 2021).…”

“…FastTree (Price et al, 2010) was used to infer gene trees per orthogroup, which were compared against the rooted species tree by Orthofinder to infer duplications/losses using a duplication-loss-coalescent model (Emms & Kelly, 2019). Kinfin v1.0 (Laetsch & Blaxter, 2017a) was used to identify orthogroups that showed evidence for gene expansion in O. edulis compared to other bivalves (Regan et al,. 2021) Functional annotation of each orthogroup was performed by searching each protein against the eukaryotic SignalP database (Petersen et al, 2011), Gene Ontology database (GO) (The Gene Ontology Consortium, 2019), and Pfam database (El-Gebali et al, 2019) using InterProScan v5.47-82.0 (Jones et al, 2014) (the top GO/Pfam/InterProScan annotation per orthogroup was recorded) and feeding the results into KinFin (Laetsch & Blaxter, 2017a).…”

“…Gene duplication is associated with adaptation during evolution (Ohno, 1970), including in bivalves (Phuangphong et al, 2021;Regan et al, 2021). To gain insights into how gene duplication influenced Ostrea evolution, we identified gene family expansions in OE_Roslin_V1 by comparison to 15 additional bivalve genomes.…”