300 Million years of coral treaders (Insecta: Heteroptera: Hermatobatidae) back to the ocean in the phylogenetic context of Arthropoda

Abstract

Among hundreds of insect families, Hermatobatidae (commonly known as coral treaders) is one of the most unique. They are small, wingless predaceous bugs in the suborder Heteroptera. Adults are almost black in colour, measuring about 5 mm in body length and 3 mm in width. Thirteen species are known from tropical coral reefs or rocky shores, but their origin and evolutionary adaptation to their unusual marine habitat were unexplored. We report here the genome and metagenome of Hermatobates lingyangjiaoensis, hitherto known only from its type locality in the South China Sea. We further reconstructed the evolutionary history and origin of these marine bugs in the broader context of Arthropoda. The dated phylogeny indicates that Hexapoda diverged from their marine sister groups approximately 498 Ma and that Hermatobatidae originated 192 Ma, indicating that they returned to an oceanic life some 300 Myr after their ancestors became terrestrial. Their origin is consistent with the recovery of tropical reef ecosystems after the end-Triassic mass extinction, which might have provided new and open niches for them to occupy and thrive. Our analyses also revealed that both the genome changes and the symbiotic bacteria might have contributed to adaptations necessary for life in the sea.

Keywords: arthropod phylogeny; genome; metagenome; origin of marine insects; phylogenomics; symbiotic bacteria.

Figure 1.

Dated phylogenomic relationships of Arthropoda. The time tree was constructed with 50 398 aligned amino acid sites. (a) Natural habitat of Hermatobates lingyangjiaoensis; (b) in situ photo of H. lingyangjiaoensis; (c) summary phylogeny and timescale of 156 Arthropoda species. Internal tree nodes are labelled with coloured dots summarizing the branch support from four maximum likelihood and four ASTRAL trees. Colour-coded square matrices show supports from different analyses for the branches that were not supported with 100% support values. Higher taxa are indicated as taxon labels on the right of the tree. Blue bars at each node represent 95% credibility intervals of the estimated date. Red lines indicate the six mass extinctions and asterisks indicate the newly sequenced transcriptomes and genomes. Species in cyan are marine. The gradient of cyan in Jurassic indicates the recovery time span of tropical reef ecosystems.

Figure 2.

Gene family expansion and contraction among genomes of H. lingyangjiaoensis and other 34 arthropod species. Expansion and contraction are indicated with symbol + and –, and the numbers indicate significantly expansion and contraction for each node and crown group. Numbers of gene families for each species are shown following specific epithet. The asterisk indicates the newly sequenced genome of H. lingyangjiaoensis. The time tree was generated with MCMCtree and the gene family expansion and contraction analyses were conducted with CAFE. Branch lengths are measured in millions of years.

Figure 3.

Functional genes of host insect and its symbiotic bacteria in different KEGG pathways. The green circle indicates functional genes of symbiotic bacteria. The orange circle indicates functional genes of insects. The black circle indicates functional genes of both host and symbiotic bacteria, and the hollow circle indicates that both host and symbiotic bacteria were lacking. Detailed gene functions associated with the aforementioned pathways were recorded in electronic supplementary material, table S15.