Genomics of a complete butterfly continent

Abstract

Never before have we had the luxury of choosing a continent, picking a large phylogenetic group of animals, and obtaining genomic data for its every species. Here, we sequence all 845 species of butterflies recorded from North America north of Mexico. Our comprehensive approach reveals the pattern of diversification and adaptation occurring in this phylogenetic lineage as it has spread over the continent, which cannot be seen on a sample of selected species. We observe bursts of diversification that generated taxonomic ranks: subfamily, tribe, subtribe, genus, and species. The older burst around 70 Mya resulted in the butterfly subfamilies, with the major evolutionary inventions being unique phenotypic traits shaped by high positive selection and gene duplications. The recent burst around 5 Mya is caused by explosive radiation in diverse butterfly groups associated with diversification in transcription and mRNA regulation, morphogenesis, and mate selection. Rapid radiation correlates with more frequent introgression of speciation-promoting and beneficial genes among radiating species. Radiation and extinction patterns over the last 100 million years suggest the following general model of animal evolution. A population spreads over the land, adapts to various conditions through mutations, and diversifies into several species. Occasional hybridization between these species results in accumulation of beneficial alleles in one, which eventually survives, while others become extinct. Not only butterflies, but also the hominids may have followed this path.Butterflies are among the most beloved animals , beautiful and harmless, they have attracted human attention since prehistoric times (1). Being one of the best-studied insects phenotypically (2), butterflies remain largely unexplored by genomics. Until recently, genomic studies of butterflies were confined to a couple of model organisms and pests, such as Heliconius, monarch, and cabbage white, with initial studies leading to groundbreaking insights into mimicry, migration, and toxin resistance (3-5). We have been expanding these efforts on butterfly genomics to cover a broader range of species (6-11). With the rapid decrease in the price of DNA sequencing and the constant development of analytical methods, the time is ripe to sequence the genomes of all butterfly species over a continent.

Evolutionary trade-offs between male secondary sexual traits revealed by a phylogeny of the hyperdiverse tribe Eumaeini (Lepidoptera: Lycaenidae)

“…Our phylogenetic results support the hypothesis that Eumaeini is monophyletic [ 1 , 25 , 44 ]. Monophyly of Eumaeini, recovered across all ML and coalescent analyses, is also supported by unique morphological characters such as elaborate androconial organs and genitalia that are quite distinct from those of other lycaenid butterflies [ 45 , 46 ].…”

“…Although lower level relationships between species and genera are statistically well supported overall, we recovered short internodes and low bootstrap values for several of the higher level relationships, suggesting insufficient sampling, rampant ILS or introgression. Nevertheless, the topology of the backbone tree is remarkably consistent with a phylogeny using whole genomes that included exemplars from 25 Eumaeini genera [44]. Thus, we suggest that the topological incongruencies we found across analyses are partly caused by ILS due to the explosive diversification of the major Eumaeini clades or introgression between the many closely related species that are sympatric.…”

De novo genome assemblies of butterflies

“…Studies of gene family evolution and gene mutation have expanded from single genes to mapping the architecture of entire genomes. Macroevolutionary studies using genomic data are now regularly being generated at impressive scales, e.g., complete class [ 1 ], continent [ 2 ], and spanning up to 500 million years [ 3 ]. As the scope of questions addressed with genomic data continues to expand, determining the effect of read length and genome completeness on results is vital.…”

Influence of the large–Z effect during contact between butterfly sister species

“…in a model where these effects are absent and mutations are individually neutral. In this work, we develop such a model and compare our results to those obtained by Cong et al [2] [4], and have, as a result, experienced multiple periods of glacial cooling and interglacial warming. During glacial periods, central Texas was subjected to severe decreases in temperature [5], which would have caused drastic, if not total isolation of sister species in southeastern and southwestern refugia; During the most recent warming period, sister species migrated into Texas, while major portions of the populations remained in refugial regions, isolated from the suture zone by large distances.…”