Positive selection in extra cellular domains in the diversification of Strigamia maritima chemoreceptors

Abstract

The recent publication of a centipede (Strigamia maritima) genome has revealed that most members of the chemosensory gene families of ionotropic (IR) and gustatory (GR) receptors do not have identifiable orthologs in insect species. In other words, the diversity of these chemoreceptors in centipedes appears to have evolved after its split from other arthropod lineages. Here we investigate the role of adaptive evolution in S. maritima chemoreceptor diversification using an approach that allows us to discuss functional aspects of such diversification. We applied codon substitution models in a phylogenetic framework to obtain the distribution of selective constraints across the different domains in the IR and GR proteins, and to assess the impact of positive selection in the evolution of these chemoreceptors. We found low selective constraints in most IR and GR duplicates and significant evidence for the presence of positively selected amino acids in two of the four IR, and in six of the GR recent specific expansions. Mapping the sites with high posterior probability of positive selection in protein structure revealed a remarkable uneven distribution of fast-evolving sites across protein domains. Most of these sites are located in extracellular fragments of these receptors, which likely participate in ligand recognition. We hypothesize that adaptive evolution in ligand-binding domains was a major force driving the functional diversification of centipede chemoreceptors.

The origin of the odorant receptor gene family in insects

“…In insects, the OR gene family evolved from within the ancestral gustatory receptor (GR) gene family ( Scott et al, 2001 ; Robertson et al, 2003 ) that extends back to ancient metazoan lineages ( Robertson, 2015 ; Saina et al, 2015 ; Eyun et al, 2017 ). ORs are absent from non-insect arthropod genomes ( Peñalva-Arana et al, 2009 ; Almeida et al, 2015 ; Gulia-Nuss et al, 2016 ; Ngoc et al, 2016 ; Eyun et al, 2017 ), and have been hypothesized to have evolved concomitant with the evolution of terrestriality in insects ( Robertson et al, 2003 ).…”

The origin of the odorant receptor gene family in insects

“…In insects, the OR gene family evolved from 61 within the ancestral gustatory receptor (GR) gene family (Scott et al, 2001;Robertson et al, 2003) that extends back to ancient metazoan lineages (Robertson, 2015;Saina et al, 63 2015;Eyun et al, 2017). ORs are absent from non-insect arthropod genomes (Peñalva-64 Arana et al, 2009;Almeida et al, 2015;Gulia-Nuss et al, 2016;Ngoc et al, 2016;Eyun 65 et al, 2017), and have been hypothesized to have evolved concomitant with the evolution 66 of terrestriality in hexapods (Robertson et al, 2003). 67…”

Relative evolutionary rates in proteins are largely insensitive to the substitution model

“…Positions which play key roles in protein functions, including those involved in protein-protein or protein-ligand interactions or those at or near active regions, tend to evolve very slowly and are highly conserved (Jack et al 2016;Echave et al 2016;Sydykova et al 2018). By contrast, sites will tend to evolve rapidly if they interact with rapidly changing external stimuli, for example if they are involved in chemosensory activity (Spielman and Wilke 2013;Almeida et al 2015), or mediate immunity, i.e. pathogen surface proteins or key regions of host immune genes (Tusche et al 2012).…”