TheNicrophorus vespilloidesgenome and methylome, a beetle with complex social behavior

Abstract

22Testing for conserved and novel mechanisms underlying phenotypic evolution requires a diversity of 23 genomes available for comparison spanning multiple independent lineages. For example, complex social 24 behavior in insects has been investigated primarily with eusocial lineages, nearly all of which are 25 Hymenoptera. If conserved genomic influences on sociality do exist, we need data from a wider range of taxa 26 that also vary in their levels of sociality. Here we present information on the genome of the subsocial beetle 27 Nicrophorus vespilloides, a species long used to investigate evolutionary questions of complex social 28 behavior. We used this genome to address two questions. First, does life history predict overlap in gene 29 models more strongly than phylogenetic groupings? Second, like other insects with highly developed social 30 behavior but unlike other beetles, does N. vespilloides have DNA methylation? We found the overlap in gene 31 models was similar between N. vespilloides and all other insect groups regardless of life history. Unlike 32 previous studies of beetles, we found strong evidence of DNA methylation, which allows this species to be 33 used to address questions about the potential role of methylation in social behavior. The addition of this 34 genome adds a coleopteran resource to answer questions about the evolution and mechanistic basis of 35 sociality. 36 37 Introduction 38Understanding phenotypic evolution necessitates investigating both the ultimate and proximate influences on 39 traits; however, these investigations require the appropriate tools. Social behavior is a particularly thorny 40 phenotype to study because of its complexity, variation, and its multi-level integration across an organism 41 (Boake et al., 2002). In addition, social behavior also often displays unusual evolutionary dynamics arising 42 from the genetic influences on interactions required for sociality (McGlothlin et al., 2010). Although single 43 genes can influence behavior (Fischman et al., 2011), social behavior is often multifaceted and can reflect a 44 complex genetic architecture (Walling et al., 2008; Mikheyev and Linksvayer, 2015) including influences 45 from epigenetic mechanisms (Cardoso et al., 2015). Genomes in particular are useful resources for 46 evolutionary questions of social behavior because they grant access to both broad scale and fine scale details 47 and mechanisms (Richards, 2015). For social behavior, while there are multiple Hymenopteran genomes 48 available to investigate fine scale detail, we lack sufficiently distantly related species to address broader 49 patterns. It is therefore important to develop genomic resources for organisms that are particularly 50 phenotypic models of social behavior but where genomic information is lacking. 51The genomes of several social insect are now available, including eusocial species such as honey 52 bees (Elsik et al., 2014), stingless bees (Kapheim et al., 2015), several ant species (Gadau et al., 2012), a 53 termite (Terrapon et al., 2...

Evolved changes in DNA methylation in response to the sustained loss of parental care in the burying beetle

“…Medium and high levels of expression did not have significantly different methylation values from each other (Figure 2b, Supp Figure 1b). These findings are consistent with previous reports of methylation residing primarily in gene bodies for this species and the presence of higher methylation levels in gene bodies of genes in plants and animals (28)(29)(30).…”

“…We performed differential methylation analysis across gene bodies to compare (1) DNA-Me between populations (evolved changes; sustained exposure to a NCENV over 30 generations) with ( 2) DNA-Me induced by a single generation of exposure to a NCENV within the FCPOP (proxy for initial response) and ( 3) DNA-Me within the NCPOP when exposed to a FCENV (population-specific responses to NCENV). As has been previously reported, not all genes in the burying beetle are methylated (28,29). Therefore, we clustered average weighted methylation values (calculated across the entire gene body), identified two distinct distributions of methylation states within genes (see Methods) and focussed our analyses on those that were classified as methylated (Supp Figure 2a, n = 4431; 39% of genes for which methylation was present for 85% of samples).…”

“…Although parental care (and its loss) has been associated with plasticity in both DNA-Me and gene expression across a number of species (23)(24)(25)(26), its role in insect DNA-Me and gene expression plasticity is still poorly understood. Burying beetles have a functioning DNA-Me system with levels of methylation that are comparable to other holometabolous insects and possess single copies of DNMT1-3 (27)(28)(29). These enzymes are highly conserved across multiple taxa and methylation occurs in actively transcribed genes suggesting important, yet still poorly understood, roles for DNA-Me in the species that carry this epigenetic modification (30,31).…”

The role of neuropeptide F in a transition to parental care

“…We used the available protein sequences of Drosophila melanogaster and Tribolium castaneum to search the genome of N. vespilloides [18] for the sequences of npf and npfr using tBLASTn (v. 2.2.25þ [19]), validated by searching against non-redundant insect proteins at NCBI using BLASTx with default settings. We obtained single copy, full-length orthologues for both npf and npfr.…”

Bacterial symbionts support larval sap feeding and adult folivory in (semi-)aquatic reed beetles

“…It is interesting to note that while most of the amino acid biosynthesis genes are located in the symbionts' chromosome, a central enzyme of the aromatic amino acid biosynthesis pathway, i.e., a bifunctional chorismate mutase/prephenate dehydratase, is encoded on the plasmid in all species, providing an explanation for the selective constraint to maintain the plasmid throughout the evolution of the symbiosis. Of the five genes that were missing in otherwise complete amino acid biosynthesis pathways in the symbiont genomes, three were previously found in beetle genomes (tyrB, ilvA, and ilvE) [19][20][21] , and the enzymatic steps were hypothesized to be taken over by the host in the aphid-Buchnera symbiosis 22 . The remaining two genes (hisC, argD) encode aminotransferases, a group of enzymes that exhibits low substrate specificity 23 .…”