Gene content evolution in the arthropods

Authors: THOMAS, GREGG W. - Indiana State University; DOHMEN, ELIAS - University Of Munster; HUGHES, DANIEL S. - Baylor College Of Medicine; MURALI, SHWETHA - Baylor College Of Medicine; Poelchau, Monica; GLASTAD, KARL - Georgia Institute Of Technology; ANSTEAD, CLARE - University Of Melbourne; AYOUB, NADIA - Washington And Lee University; BATTERHAM, PHILLIP - University Of Melbourne; BELLAIR, MICHELLE - Baylor College Of Medicine; Childers, Christopher; Duan, Jian; Gundersen-Rindal, Dawn; Handler, Alfred - Al; Hunter, Wayne; Scully, Erin; Hackett, Kevin

Submitted to: Genome Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/19/2019
Publication Date: 1/23/2020
Citation: Thomas, G.C., Dohmen, E., Hughes, D.T., Murali, S.C., Poelchau, M.F., Glastad, K., Anstead, C.A., Ayoub, N.A., Batterham, P., Bellair, M., Childers, C., Duan, J.J., Gundersen, D.E., Handler, A.M., Hunter, W.B., Scully, E.D., Hackett, K.J., et all. 2020. Gene content evolution in the arthropods. Genome Biology. 21:15. https://doi.org/10.1186/s13059-019-1925-7.
DOI: https://doi.org/10.1186/s13059-019-1925-7

Interpretive Summary: Arthropods - animals such as butterflies, flies, spiders, centipedes, and crustaceans - are an incredibly diverse and abundant group. Arthropods include both agricultural and veterinary pests, as well as beneficial pollinators. Scientists wish to understand how this incredible diversity has arisen. One approach is to analyze genome sequences across the range of this branch of the evolutionary tree. In this paper, the authors analyze the genome sequences of 76 arthropod species representing 21 orders spanning over 500 million years of evolution. From the protein sequences encoded in these genomes, they produce a new, comprehensive phylogenetic tree - which allows them to ask several sets of questions. First, what novel 'families' of genes have arisen, and when did they arise? Second, what changes in protein domain content - which gives clues to protein function - occurred? Finally, how does DNA methylation, which affects how genes are regulated, differ across the arthropods? During early arthropod evolution, they find that different sets of gene families became important - 147 new gene families emerged at the Last Insect Common Ancestor, including genes likely related to wing generation; 10 emergent gene families in the Last Holometabolous Common Ancestor (insects that go through distinct larval, pupal, and adult stages); and an astonishing number of emergent gene families - 1,038 - in the last Lepitopteran common ancestor (insects including butterflies). Leaf-cutter ants showed high rates of gene gain and loss, and domain re-arrangements; and spiders show surprisingly high rates of DNA methylation. Together, scientists will be able to use the results of these analyses to understand how new traits evolved in the arthropods, and to make new hypotheses about how insects evolved.

Technical Abstract: Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods. Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality and chemoperception. These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.