skip to main content


Title: Expansion and Accelerated Evolution of 9-Exon Odorant Receptors in Polistes Paper Wasps
Abstract Independent origins of sociality in bees and ants are associated with independent expansions of particular odorant receptor (OR) gene subfamilies. In ants, one clade within the OR gene family, the 9-exon subfamily, has dramatically expanded. These receptors detect cuticular hydrocarbons (CHCs), key social signaling molecules in insects. It is unclear to what extent 9-exon OR subfamily expansion is associated with the independent evolution of sociality across Hymenoptera, warranting studies of taxa with independently derived social behavior. Here, we describe OR gene family evolution in the northern paper wasp, Polistes fuscatus, and compare it to four additional paper wasp species spanning ∼40 million years of evolutionary divergence. We find 200 putatively functional OR genes in P. fuscatus, matching predictions from neuroanatomy, and more than half of these are in the 9-exon subfamily. Most OR gene expansions are tandemly arrayed at orthologous loci in Polistes genomes, and microsynteny analysis shows species-specific gain and loss of 9-exon ORs within tandem arrays. There is evidence of episodic positive diversifying selection shaping ORs in expanded subfamilies. Values of omega (dN/dS) are higher among 9-exon ORs compared to other OR subfamilies. Within the Polistes OR gene tree, branches in the 9-exon OR clade experience relaxed negative (relaxed purifying) selection relative to other branches in the tree. Patterns of OR evolution within Polistes are consistent with 9-exon OR function in CHC perception by combinatorial coding, with both natural selection and neutral drift contributing to interspecies differences in gene copy number and sequence.  more » « less
Award ID(s):
1750394
NSF-PAR ID:
10273532
Author(s) / Creator(s):
; ; ; ;
Editor(s):
Agashe, Deepa
Date Published:
Journal Name:
Molecular Biology and Evolution
ISSN:
0737-4038
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Cognitive abilities can vary dramatically among species. The relative importance of social and ecological challenges in shaping cognitive evolution has been the subject of a long-running and recently renewed debate, but little work has sought to understand the selective dynamics underlying the evolution of cognitive abilities. Here, we investigate recent selection related to cognition in the paper waspPolistes fuscatus—a wasp that has uniquely evolved visual individual recognition abilities. We generate high quality de novo genome assemblies and population genomic resources for multiple species of paper wasps and use a population genomic framework to interrogate the probable mode and tempo of cognitive evolution. Recent, strong, hard selective sweeps inP. fuscatuscontain loci annotated with functions in long-term memory formation, mushroom body development, and visual processing, traits which have recently evolved in association with individual recognition. The homologous pathways are not under selection in closely related wasps that lack individual recognition. Indeed, the prevalence of candidate cognition loci within the strongest selective sweeps suggests that the evolution of cognitive abilities has been among the strongest selection pressures inP. fuscatus’ recent evolutionary history. Detailed analyses of selective sweeps containing candidate cognition loci reveal multiple cases of hard selective sweeps within the last few thousand years on de novo mutations, mainly in noncoding regions. These data provide unprecedented insight into some of the processes by which cognition evolves.

     
    more » « less
  2. Parrish, Colin R. (Ed.)
    ABSTRACT Bracoviruses (BVs) are endogenized nudiviruses in parasitoid wasps of the microgastroid complex (family Braconidae). Microgastroid wasps have coopted nudivirus genes to produce replication-defective virions that females use to transfer virulence genes to parasitized hosts. The microgastroid complex further consists of six subfamilies and ∼50,000 species but current understanding of BV gene inventories and organization primarily derives from analysis of two wasp species in the subfamily Microgastrinae ( Microplitis demolitor and Cotesia congregata ) that produce M. demolitor BV (MdBV) and C. congregata BV (CcBV). Notably, several genomic features of MdBV and CcBV remain conserved since divergence of M. demolitor and C. congregata ∼53 million years ago (MYA). However, it is unknown whether these conserved traits more broadly reflect BV evolution, because no complete genomes exist for any microgastroid wasps outside the Microgastrinae. In this regard, the subfamily Cheloninae is of greatest interest because it diverged earliest from the Microgastrinae (∼85 MYA) after endogenization of the nudivirus ancestor. Here, we present the complete genome of Chelonus insularis , which is an egg-larval parasitoid in the Cheloninae that produces C. insularis BV (CinsBV). We report that the inventory of nudivirus genes in C. insularis is conserved but are dissimilarly organized compared to M. demolitor and C. congregata . Reciprocally, CinsBV proviral segments share organizational features with MdBV and CcBV but virulence gene inventories exhibit almost no overlap. Altogether, our results point to the functional importance of a conserved inventory of nudivirus genes and a dynamic set of virulence genes for the successful parasitism of hosts. Our results also suggest organizational features previously identified in MdBV and CcBV are likely not essential for BV virion formation. IMPORTANCE Bracoviruses are a remarkable example of virus endogenization, because large sets of genes from a nudivirus ancestor continue to produce virions that thousands of wasp species rely upon to parasitize hosts. Understanding how these genes interact and have been coopted by wasps for novel functions is of broad interest in the study of virus evolution. This work characterizes bracovirus genome components in the parasitoid wasp Chelonus insularis , which together with existing wasp genomes captures a large portion of the diversity among wasp species that produce bracoviruses. Results provide new information about how bracovirus genome components are organized in different wasps while also providing additional insights on key features required for function. 
    more » « less
  3. Abstract

    The family Mutillidae (Hymenoptera) is a species‐rich group of aculeate wasps that occur worldwide. The higher‐level classification of the family has historically been controversial due, in part, to the extreme sexual dimorphism exhibited by these insects and their morphological similarity to other wasp taxa that also have apterous females. Modern hypotheses on the internal higher classification of Mutillidae have been exclusively based on morphology and, further, they include Myrmosinae as a mutillid subfamily. In contrast, several molecular‐based family‐level studies of Aculeata recovered Myrmosinae as a nonmutillid taxon. To test the validity of these morphology‐based classifications and the phylogenetic placement of the controversial taxon Myrmosinae, a phylogenomic study of Mutillidae was conducted using ultraconserved elements (UCEs). All currently recognized subfamilies and tribes of Mutillidae were represented in this study using 140 ingroup taxa. The maximum likelihood criterion (ML) and the maximum parsimony criterion (MP) were used to infer the phylogenetic relationships within the family and related taxa using an aligned data set of 238,764 characters; the topologies of these respective analyses were largely congruent. The modern higher classification of Mutillidae, based on morphology, is largely congruent with the phylogenomic results of this study at the subfamily level, whereas the tribal classification is poorly supported. The subfamily Myrmosinae was recovered as sister to Sapygidae in the ML analysis and sister to Sapygidae + Pompilidae in the MP analysis; it is consequently raised to the family level, Myrmosidae,stat.nov.The two constituent tribes of Myrmosidae are raised to the subfamily level, Kudakrumiinae,stat.nov., and Myrmosinae,stat.nov.All four recognized tribes of Mutillinae were found to be non‐monophyletic; three additional mutilline clades were recovered in addition to Ctenotillini, Mutillini, Smicromyrmini, and Trogaspidiini sensu stricto. Three new tribes are erected for members of these clades: Pristomutillini Waldren,trib.nov., Psammothermini Waldren,trib.nov., and Zeugomutillini Waldren,trib.nov.All three recognized tribes of Sphaeropthalminae were found to be non‐monophyletic; six additional sphaeropthalmine clades were recovered in addition to Dasymutillini, Pseudomethocini, and Sphaeropthalmini sensu stricto. The subtribe Ephutina of Mutillinae: Mutillini was found to be polyphyletic, with theEphutagenus‐group recovered within Sphaeropthalminae and theOdontomutillagenus‐group recovered as sister to Myrmillinae + Mutillinae. Consequently, the subtribe Ephutina is transferred from Mutillinae: Mutillini and is raised to a tribe within Sphaeropthalminae, Ephutini,stat.nov.Further, the taxon Odontomutillinae,stat.nov., is raised from a synonym of Ephutina to the subfamily level. The sphaeropthalmine tribe Pseudomethocini was found to be polyphyletic, with the subtribe Euspinoliina recovered as a separate clade in Sphaeropthalminae; consequently, Euspinoliina is raised to a tribe, Euspinoliini,stat.nov., in Sphaeropthalminae. The dasylabrine tribe Apteromutillini was recovered within Dasylabrini and is proposed as a new synonym of Dasylabrinae. Finally, dating analyses were conducted to infer the ages of the Pompiloidea families (Mutillidae, Myrmosidae, Pompilidae, and Sapygidae) and the ages of the Mutillidae subfamilies and tribes.

     
    more » « less
  4. Abstract

    Contamination of a genetic sample with DNA from one or more nontarget species is a continuing concern of molecular phylogenetic studies, both Sanger sequencing studies and next-generation sequencing studies. We developed an automated pipeline for identifying and excluding likely cross-contaminated loci based on the detection of bimodal distributions of patristic distances across gene trees. When contamination occurs between samples within a data set, a comparison between a contaminated sample and its contaminant taxon will yield bimodal distributions with one peak close to zero patristic distance. This new method does not rely on a priori knowledge of taxon relatedness nor does it determine the causes(s) of the contamination. Exclusion of putatively contaminated loci from a data set generated for the insect family Cicadidae showed that these sequences were affecting some topological patterns and branch supports, although the effects were sometimes subtle, with some contamination-influenced relationships exhibiting strong bootstrap support. Long tip branches and outlier values for one anchored phylogenomic pipeline statistic (AvgNHomologs) were correlated with the presence of contamination. While the anchored hybrid enrichment markers used here, which target hemipteroid taxa, proved effective in resolving deep and shallow level Cicadidae relationships in aggregate, individual markers contained inadequate phylogenetic signal, in part probably due to short length. The cleaned data set, consisting of 429 loci, from 90 genera representing 44 of 56 current Cicadidae tribes, supported three of the four sampled Cicadidae subfamilies in concatenated-matrix maximum likelihood (ML) and multispecies coalescent-based species tree analyses, with the fourth subfamily weakly supported in the ML trees. No well-supported patterns from previous family-level Sanger sequencing studies of Cicadidae phylogeny were contradicted. One taxon (Aragualna plenalinea) did not fall with its current subfamily in the genetic tree, and this genus and its tribe Aragualnini is reclassified to Tibicininae following morphological re-examination. Only subtle differences were observed in trees after the removal of loci for which divergent base frequencies were detected. Greater success may be achieved by increased taxon sampling and developing a probe set targeting a more recent common ancestor and longer loci. Searches for contamination are an essential step in phylogenomic analyses of all kinds and our pipeline is an effective solution. [Auchenorrhyncha; base-composition bias; Cicadidae; Cicadoidea; Hemiptera; phylogenetic conflict.]

     
    more » « less
  5. A molecular phylogeny and a review of family-group classification are presented for 137 species (ca. 125 genera) of the insect family Cicadidae, the true cicadas, plus two species of hairy cicadas (Tettigarctidae) and two outgroup species from Cercopidae. Five genes, two of them mitochondrial, comprise the 4992 base-pair molecular dataset. Maximum-likelihood and Bayesian phylogenetic results are shown, including analyses to address potential base composition bias. Tettigarcta is confirmed as the sister-clade of the Cicadidae and support is found for three subfamilies identified in an earlier morphological cladistic analysis. A set of paraphyletic deep-level clades formed by African genera are together named as Tettigomyiinae n. stat. Taxonomic reassignments of genera and tribes are made where morphological examination confirms incorrect placements suggested by the molecular tree, and 11 new tribes are defined (Arenopsaltriini n. tribe, Durangonini n. tribe, Katoini n. tribe, Lacetasini n. tribe, Macrotristriini n. tribe, Malagasiini n. tribe, Nelcyndanini n. tribe, Pagiphorini n. tribe, Pictilini n. tribe, Psaltodini n. tribe, and Selymbriini n. tribe). Tribe Tacuini n. syn. is synonymized with Cryptotympanini, and Tryellina n. syn. is synonymized with an expanded Tribe Lamotialnini. Tribe Hyantiini n. syn. is synonymized with Fidicinini. Tribe Sinosenini is transferred to Cicadinae from Cicadettinae, Cicadatrini is moved to Cicadettinae from Cicadinae, and Ydiellini and Tettigomyiini are transferred to Tettigomyiinae n. stat from Cicadettinae. While the subfamily Cicadinae, historically defined by the presence of timbal covers, is weakly supported in the molecular tree, high taxonomic rank is not supported for several earlier clades based on unique morphology associated with sound production. 
    more » « less