Evolution and Diversification Dynamics of Butterflies

Abstract

Butterflies are a diverse and charismatic insect group that are thought to have diversified via coevolution with plants and in response to dispersals following key geological events. These hypotheses have been poorly tested at the macroevolutionary scale because a comprehensive phylogenetic framework and datasets on global distributions and larval hosts of butterflies are lacking. We sequenced 391 genes from nearly 2,000 butterfly species to construct a new, phylogenomic tree of butterflies representing 92% of all genera and aggregated global distribution records and larval host datasets. We found that butterflies likely originated in what is now the Americas, ~100 Ma, shortly before the Cretaceous Thermal Maximum, then crossed Beringia and diversified in the Paleotropics. The ancestor of modern butterflies likely fed on Fabaceae, and most extant families were present before the K/Pg extinction. The majority of butterfly dispersals occurred from the tropics (especially the Neotropics) to temperate zones, largely supporting a "cradle" pattern of diversification. Surprisingly, host breadth changes and shifts to novel host plants had only modest impacts.

Diversification is correlated with temperature in white and sulfur butterflies

“…Subfamilial relationships were strongly supported (UFBoot and aLRT >95%) in general, but support for the position of Pseudopontiinae, which we recovered as the sister group to Pierinae, was low (UFBoot =75.2, SHaLRT = 77). This corroborates the results of Kawahara et al (24) and Espeland et al (41), based on 391 loci, but not of Chazot et al (42), which used 9 loci (Fig. 1).…”

“…This study provides a robust phylogenetic framework of pierid butterflies and a foundation for testing many macroevolutionary questions. We show, with strong support (UFBoot and SH- aLRT = 100), that Dismorphiinae are sister to a clade containing Coliadinae, Pseudopontiinae, and Pierinae, in agreement with Wahlberg et al (36) and Kawahara et al (24). All tribal relationships of Pierinae were strongly supported and differ from previous studies (24, 36, 42).…”

“…Wheat and colleagues found evidence in Pieridae for the signature of escalating arms races via the coupled evolution of plant chemical defenses (glucosinolates) and detoxification mechanisms (nitrite-specifier proteins) (22), as well as other key innovations involving chemical defenses derived from gene and genome duplications (23). A genus-level phylogenetic investigation of all butterflies by Kawahara et al (24) found limited evidence that host plant switches affect diversification rates. Our exploratory ancestral state reconstruction of plant orders did not uncover any striking host shifts that coincided with diversification rate shifts, but we did not conduct any direct analyses to test for effects of host plants on diversification.…”

“…The sequences of Warren-Gash et al (39) were made available on GenBank after we used GeneDumper, so we downloaded those sequences from the database for species not already in our molecular dataset. We also incorporated sequences from other targeted studies (38,41), and used genomes and transcriptomes assembled to the BUTTERFLY1.0 probe kit in Kawahara et al (24) (including two as outgroups) (Dataset S6). There were 15 species for which we created chimeras by adding cytochrome oxidase subunit 1 (COI) from one sample to another with more loci available but no COI (see Dataset S6 for more details).…”

“…Prior investigations have found strong evidence for reciprocal adaptations between Pierinae butterflies and their host plants as predicted by an escape-and-radiate coevolutionary scenario (22, 23). However, an extensive study examining evolutionary patterns of host use across all butterflies found weak evidence for coevolution in many clades (24). Host plants are just one factor that might affect insect diversification rates; less attention has been paid to the role of climate.…”