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Positive Selection in Extra Cellular Domains in the Diversification Of ORIGINAL RESEARCH published: 22 July 2015 doi: 10.3389/fevo.2015.00079 Positive selection in extra cellular domains in the diversification of Strigamia maritima chemoreceptors Francisca C. Almeida 1 † ‡, Alejandro Sánchez-Gracia 1‡, Kimberly K. O. Walden 2, Hugh M. Robertson 2 and Julio Rozas 1* 1 Departament de Genètica and Institut de Recerca de la Biodiversitat, Universitat de Barcelona, Barcelona, Spain, 2 Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL, USA Edited by: William Benjamin Walker, The recent publication of a centipede (Strigamia maritima) genome has revealed that Swedish University of Agricultural Sciences, Sweden most members of the chemosensory gene families of ionotropic (IR) and gustatory (GR) Reviewed by: receptors do not have identifiable orthologs in insect species. In other words, the diversity Jeremy J. Heath, of these chemoreceptors in centipedes appears to have evolved after its split from other North Carolina State University, USA Jing-Jiang Zhou, arthropod lineages. Here we investigate the role of adaptive evolution in S. maritima Rothamsted Research, UK chemoreceptor diversification using an approach that allows us to discuss functional *Correspondence: aspects of such diversification. We applied codon substitution models in a phylogenetic Julio Rozas, framework to obtain the distribution of selective constraints across the different domains Departament de Genètica, Universitat de Barcelona, Av. Diagonal 643, in the IR and GR proteins, and to assess the impact of positive selection in the evolution of Barcelona 08028, Spain these chemoreceptors. We found low selective constraints in most IR and GR duplicates [email protected] and significant evidence for the presence of positively selected amino acids in two of †Present Address: Francisca C. Almeida, the four IR, and in six of the GR recent specific expansions. Mapping the sites with Departamento de Ecología, Genética high posterior probability of positive selection in protein structure revealed a remarkable y Evolución, Consejo Nacional de uneven distribution of fast-evolving sites across protein domains. Most of these sites are Investigaciones Científicas y Tecnológicas, Universidad de Buenos located in extracellular fragments of these receptors, which likely participate in ligand Aires, Buenos Aires, Argentina recognition. We hypothesize that adaptive evolution in ligand-binding domains was a ‡These authors have contributed major force driving the functional diversification of centipede chemoreceptors. equally to this work. Keywords: positive selection, functional domains, chemosensory function, gustatory receptor, ionotropic receptor Specialty section: This article was submitted to Chemical Ecology, Introduction a section of the journal Frontiers in Ecology and Evolution The chemosensory system of arthropods is an interesting subject to study evolution due to its Received: 16 April 2015 adaptive value. Chemosensation is necessary for finding food, avoiding predators, and locating Accepted: 07 July 2015 and choosing mates. The system is composed of proteins encoded by small to medium-sized Published: 22 July 2015 gene families of two main types: chemosensory (membrane) receptors and ligand-binding Citation: proteins (Pelosi et al., 2006; Sánchez-Gracia et al., 2009, 2011; Touhara and Vosshall, 2009). Almeida FC, Sánchez-Gracia A, First studied in Drosophila melanogaster, three chemoreceptor gene families were identified: Walden KKO, Robertson HM and Olfactory receptors (OR), Gustatory receptors (GR), and Ionotropic receptors (IR) (Robertson Rozas J (2015) Positive selection in et al., 2003; Benton et al., 2009). With the sequencing of other arthropod genomes, it became extra cellular domains in the diversification of Strigamia maritima evident that the ORs are unique to insects (Peñalva-Arana et al., 2009; Chipman et al., 2014). chemoreceptors. Members of the GR and IR gene families were, in contrast, found in all arthropod genomes Front. Ecol. Evol. 3:79. sequenced so far. In fact, the IRs and GRs seem to have an even older origin; they are present doi: 10.3389/fevo.2015.00079 in non-arthropod animals, but GRs probably did not always have a chemosensory function Frontiers in Ecology and Evolution | www.frontiersin.org 1 July 2015 | Volume 3 | Article 79 Almeida et al. Chemoreceptor evolution in Strigamia maritime (Croset et al., 2010; Rytz et al., 2013; Saina et al., 2015; Hugh for an acquired beneficial mutation. In the latter case, the copy Robertson unpublished). In D. melanogaster, olfaction, or the may be maintained due to its functional differentiation in a perception of airborne or volatile chemicals, is mediated by the process called neofunctionalization (Ohno, 1970). Another, non- ORs. GRs are implicated in the perception of soluble chemicals exclusive explanation for the lineage specific expansions observed and CO2, while IRs have been implicated in the detection of in the chemosensory gene families is the stochastic nature of both soluble and airborne cues (Vosshall and Stocker, 2007; Rytz the gene birth and death process. According to this hypothesis, et al., 2013). Arthropods have a marine ancestry, but there were the maintenance, and loss of duplicated gene copies can be several independent invasions of land, such as in the Chelicerates, mostly explained by an entirely random process dubbed random Myriapods, and Insects (Rota-Stabelli et al., 2013). Since the ORs genomic drift, which is characterized by only two parameters: are not present in the Chelicerates and Myriapods (Chipman gene birth and death rates (Nei, 2007; Nei et al., 2008). Here et al., 2014; Frías-López et al., 2015; Hugh Robertson unpublished we make use of state-of-the-art phylogenetic methods that results, Julio Rozas unpublished results), an evident question is allow for the exploration of genomic data to understand very which genes encode receptors for air-borne cues in these land specific details of gene family functional evolution. We used arthropods. these methods to test whether positive selection was involved Here, we begin to investigate this question by analyzing the in GR and IR paralog divergence and in this way evaluate evolution of the GR and IR families in a myriapod that has the role of selection in the evolution of these gene families in recently had its genome sequence published: Strigamia maritima S. maritima. This approach permits the identification of amino (Chipman et al., 2014). This species is found along the coastline acid residues likely under positive selection and consequently of northwestern Europe and has been used as a model system in which gene regions and amino acid sites are under selective developmental studies (Kettle et al., 2003; Arthur and Chipman, pressure for diversification. This study is a fundamental genomics 2005; Chipman and Akam, 2008; Green and Akam, 2013). contribution to the functional aspects of the chemosensory Interestingly, it belongs to a centipede Order (Geophilimorphs) receptors of S. maritima and lays the ground for further that includes animals that have completely lost their eyes, which examination of S. maritima’s chemosensory system through suggests they rely heavily on other sensory systems. A search for experimental approaches. GR and IR orthologs in the S. maritima genome identified 76 GRs (13 of which are pseudogenes) and 54 IRs (3 of which are Materials and Methods pseudogenes) (Chipman et al., 2014). These numbers are well within the range of gene family members in other arthropod Dataset species. In both families, however, only a few 1:1 orthologous All gene sequences used in this study were manually curated by us relationships were found with other arthropod chemoreceptors and published in Chipman et al. (2014). In brief, we ran a number (Chipman et al., 2014). Instead, phylogenetic analyses for each of similarity searches on the S. maritima genome to identify chemoreceptor family revealed that all S. maritima GR and candidate S. maritima GR and IR genes. We then superimposed most IR genes clustered together in a single clade without the results of these searches, available EST information, and the close relationships to orthologs in other arthropod species. automated gene predictions on the genome to manually annotate This result suggests that the observed diversity of myriapod each chemosensory gene and obtain the dataset we used in the chemosensory receptors evolved after this lineage split from its present study (see details in Chipman et al., 2014; S. maritima last common ancestor with other arthropods. The only genes IR and GR CDS sequences are included in the Supplementary with an identifiable candidate ortholog in other arthropods Material). were three IRs (SmarIR25a, SmarIR8a, and SmarIR49) with The methodological approach we used herein to detect signs antennal expression in D. melanogaster, which points to a role of positive selection depends on sequence variation and its in olfaction in flies (Chipman et al., 2014). Namely, IR25a is accuracy is reduced if it is applied to very divergent paralogs. a highly conserved gene in Protostomia and appears to have To circumvent this problem, we first identified recent clades kept its chemosensory function throughout the evolution of this based on synonymous divergence in both the GR and the IR group (Croset et al., 2010). In fact, this gene is broadly expressed gene families within which separate analyses would be carried in Drosophila olfactory tissues and might represent a common out (Figure 1). For that, we first obtained
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