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The first molecular phylogeny of Strepsiptera (Insecta) reveals an early burst of molecular evolution correlated with the transition to endoparasitism.

ABSTRACT: A comprehensive model of evolution requires an understanding of the relationship between selection at the molecular and phenotypic level. We investigate this in Strepsiptera, an order of endoparasitic insects whose evolutionary biology is poorly studied. We present the first molecular phylogeny of Strepsiptera, and use this as a framework to investigate the association between parasitism and molecular evolution. We find evidence of a significant burst in the rate of molecular evolution in the early history of Strepsiptera. The evolution of morphological traits linked to parasitism is significantly correlated with the pattern in molecular rate. The correlated burst in genotypic-phenotypic evolution precedes the main phase of strepsipteran diversification, which is characterised by the return to a low and even molecular rate, and a period of relative morphological stability. These findings suggest that the transition to endoparasitism led to relaxation of selective constraint in the strepsipteran genome. Our results indicate that a parasitic lifestyle can affect the rate of molecular evolution, although other causal life-history traits correlated with parasitism may also play an important role.

SUBMITTER: McMahon DP

PROVIDER: S-EPMC3125182 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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The first molecular phylogeny of Strepsiptera (Insecta) reveals an early burst of molecular evolution correlated with the transition to endoparasitism.

McMahon Dino P DP Hayward Alexander A Kathirithamby Jeyaraney J

PloS one 20110628 6

A comprehensive model of evolution requires an understanding of the relationship between selection at the molecular and phenotypic level. We investigate this in Strepsiptera, an order of endoparasitic insects whose evolutionary biology is poorly studied. We present the first molecular phylogeny of Strepsiptera, and use this as a framework to investigate the association between parasitism and molecular evolution. We find evidence of a significant burst in the rate of molecular evolution in the ea ...[more]

PMID: 21738621

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Project description:BACKGROUND:Maternal care (egg-nymph guarding behavior) has been recorded in some genera of Acanthosomatidae. However, the origin of the maternal care in the family has remained unclear due to the lack of phylogenetic hypotheses. Another reproductive mode is found in non-caring species whose females smear their eggs before leaving them. They possess pairs of complex organs on the abdominal venter called Pendergrast's organ (PO) and spread the secretion of this organ onto each egg with their hind legs, which is supposed to provide a protective function against enemies. Some authors claim that the absence of PO may be associated with the presence of maternal care. No study, however, has tested this hypothesis of a correlated evolution between the two traits. RESULTS:We reconstructed the molecular phylogeny of the subfamily Acanthosomatinae using five genetic markers sequenced from 44 species and one subspecies with and without maternal care. Eight additional species from the other two acanthosomatid subfamilies were included as outgroups. Our results indicated that maternal care has evolved independently at least three times within Acanthosomatinae and once in the outgroup species. Statistical tests for correlated evolution showed that the presence of maternal care is significantly correlated with the secondary loss or reduction of PO. Ancestral state reconstruction for the node of Acanthosoma denticaudum (a non-caring species in which egg smearing with developed POs occurs) and A. firmatum (a caring species with reduced POs) suggested egg smearing was still present in their most recent common ancestor and that maternal care in A. firmatum has evolved relatively recently. CONCLUSIONS:We showed that maternal care is an apomorphic trait that has arisen multiple times from the presence of PO within the subfamily Acanthosomatinae. The acquisition of maternal care is correlated with the reduction or loss of PO, which suggests an evolutionary trade-off between the two traits resulting from physiological costs. This prediction also implies that presence of maternal care can be highly expected for those groups lacking behavioral data, which invariably also lack the organ. No secondary loss of maternal care was detected in the present tree. We suggest that the loss of maternal care may be suppressed due to the vulnerability of the PO-free condition, which thus maintains maternal care.

Project description:BackgroundYponomeutoidea, one of the early-diverging lineages of ditrysian Lepidoptera, comprise about 1,800 species worldwide, including notable pests and insect-plant interaction models. Yponomeutoids were one of the earliest lepidopteran clades to evolve external feeding and to extensively colonize herbaceous angiosperms. Despite the group's economic importance, and its value for tracing early lepidopteran evolution, the biodiversity and phylogeny of Yponomeutoidea have been relatively little studied.Methodology/principal findingsEight nuclear genes (8 kb) were initially sequenced for 86 putative yponomeutoid species, spanning all previously recognized suprageneric groups, and 53 outgroups representing 22 families and 12 superfamilies. Eleven to 19 additional genes, yielding a total of 14.8 to 18.9 kb, were then sampled for a subset of taxa, including 28 yponomeutoids and 43 outgroups. Maximum likelihood analyses were conducted on data sets differing in numbers of genes, matrix completeness, inclusion/weighting of synonymous substitutions, and inclusion/exclusion of "rogue" taxa. Monophyly for Yponomeutoidea was supported very strongly when the 18 "rogue" taxa were excluded, and moderately otherwise. Results from different analyses are highly congruent and relationships within Yponomeutoidea are well supported overall. There is strong support overall for monophyly of families previously recognized on morphological grounds, including Yponomeutidae, Ypsolophidae, Plutellidae, Glyphipterigidae, Argyresthiidae, Attevidae, Praydidae, Heliodinidae, and Bedelliidae. We also assign family rank to Scythropiinae (Scythropiidae stat. rev.), which in our trees are strongly grouped with Bedelliidae, in contrast to all previous proposals. We present a working hypothesis of among-family relationships, and an informal higher classification. Host plant family associations of yponomeutoid subfamilies and families are non-random, but show no trends suggesting parallel phylogenesis. Our analyses suggest that previous characterizations of yponomeutoids as predominantly Holarctic were based on insufficient sampling.Conclusions/significanceWe provide the first robust molecular phylogeny for Yponomeutoidea, together with a revised classification and new insights into their life history evolution and biogeography.

Project description:BackgroundStrepsiptera are an unusual group of sexually dimorphic, entomophagous parasitoids whose evolutionary origins remain elusive. The lineage leading to Mengenilla australiensis (Family Mengenillidae) is the sister group to all remaining extant strepsipterans. It is unique in that members of this family have retained a less derived condition, where females are free-living from pupation onwards, and are structurally much less simplified. We sequenced almost the entire mitochondrial genome of M. australiensis as an important comparative data point to the already available genome of its distant relative Xenos vesparum (Family Xenidae). This study represents the first in-depth comparative mitochondrial genomic analysis of Strepsiptera.ResultsThe partial genome of M. australiensis is presented as a 13421 bp fragment, across which all 13 protein-coding genes (PCGs), 2 ribosomal RNA (rRNA) genes and 18 transfer RNA (tRNA) sequences are identified. Two tRNA translocations disrupt an otherwise ancestral insect mitochondrial genome order. A+T content is measured at 84.3%, C-content is also very skewed. Compared with M. australiensis, codon bias in X. vesparum is more balanced. Interestingly, the size of the protein coding genome is truncated in both strepsipterans, especially in X. vesparum which, uniquely, has 4.3% fewer amino acids than the average holometabolan complement. A revised assessment of mitochondrial rRNA secondary structure based on comparative structural considerations is presented for M. australiensis and X. vesparum.ConclusionsThe mitochondrial genome of X. vesparum has undergone a series of alterations which are probably related to an extremely derived lifestyle. Although M. australiensis shares some of these attributes; it has retained greater signal from the hypothetical most recent common ancestor (MRCA) of Strepsiptera, inviting the possibility that a shift in the mitochondrial selective environment might be related to the specialization accompanying the evolution of a small, morphologically simplified completely host-dependent lifestyle. These results provide useful insights into the nature of the evolutionary transitions that accompanied the emergence of Strepsiptera, but we emphasize the need for adequate sampling across the order in future investigations concerning the extraordinary developmental and evolutionary origins of this group.

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The first molecular phylogeny of Strepsiptera (Insecta) reveals an early burst of molecular evolution correlated with the transition to endoparasitism.

Publications

The first molecular phylogeny of Strepsiptera (Insecta) reveals an early burst of molecular evolution correlated with the transition to endoparasitism.

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