Butterflies are a diverse and charismatic insect group that are thought to have evolved with plants and dispersed throughout the world in response to key geological events. However, these hypotheses have not been extensively tested because a comprehensive phylogenetic framework and datasets for butterfly larval hosts and global distributions are lacking. We sequenced 391 genes from nearly 2,300 butterfly species, sampled from 90 countries and 28 specimen collections, to reconstruct a new phylogenomic tree of butterflies representing 92% of all genera. Our phylogeny has strong support for nearly all nodes and demonstrates that at least 36 butterfly tribes require reclassification. Divergence time analyses imply an origin ~100 million years ago for butterflies and indicate that all but one family were present before the K/Pg extinction event. We aggregated larval host datasets and global distribution records and found that butterflies are likely to have first fed on Fabaceae and originated in what is now the Americas. Soon after the Cretaceous Thermal Maximum, butterflies crossed Beringia and diversified in the Palaeotropics. Our results also reveal that most butterfly species are specialists that feed on only one larval host plant family. However, generalist butterflies that consume two or more plant families usually feed on closely related plants.
Male butterflies in the hyperdiverse tribe Eumaeini possess an unusually complex and diverse repertoire of secondary sexual characteristics involved in pheromone production and dissemination. Maintaining multiple sexually selected traits is likely to be metabolically costly, potentially resulting in trade-offs in the evolution of male signals. However, a phylogenetic framework to test hypotheses regarding the evolution and maintenance of male sexual traits in Eumaeini has been lacking. Here, we infer a comprehensive, time-calibrated phylogeny from 379 loci for 187 species representing 91% of the 87 described genera. Eumaeini is a monophyletic group that originated in the late Oligocene and underwent rapid radiation in the Neotropics. We examined specimens of 818 of the 1096 described species (75%) and found that secondary sexual traits are present in males of 91% of the surveyed species. Scent pads and scent patches on the wings and brush organs associated with the genitalia were probably present in the common ancestor of Eumaeini and are widespread throughout the tribe. Brush organs and scent pads are negatively correlated across the phylogeny, exhibiting a trade-off in which lineages with brush organs are unlikely to regain scent pads and vice versa . In contrast, scent patches seem to facilitate the evolution of scent pads, although they are readily lost once scent pads have evolved. Our results illustrate the complex interplay between natural and sexual selection in the origin and maintenance of multiple male secondary sexual characteristics and highlight the potential role of sexual selection spurring diversification in this lineage.
Males of many butterfly species secrete long-lasting mating plugs to prevent their mates from copulating with other males, thus ensuring their sperm will fertilize all future eggs laid. Certain species have further developed a greatly enlarged, often spectacular, externalized plug, termed a sphragis. This distinctive structure results from complex adaptations in both male and female genitalia and is qualitatively distinct from the amorphous, internal mating plugs of other species. Intermediate conditions between internal plug and external sphragis are rare. The term sphragis has often been misunderstood in recent years, hence we provide a formal definition based on accepted usage throughout most of the last century. Despite it being a highly apparent trait, neither the incidence nor diversity of the sphragis has been systematically documented. We record a sphragis or related structure in 273 butterfly species, representing 72 species of Papilionidae in 13 genera, and 201 species of Nymphalidae in 9 genera. These figures represent respectively, 13% of Papilionidae, 3% of Nymphalidae, and 1% of known butterfly species. A well-formed sphragis evolved independently in at least five butterfly subfamilies, with a rudimentary structure also occurring in an additional subfamily. The sphragis is probably the plesiomorphic condition in groups such as Parnassius (Papilionidae: Parnassiinae) and many Acraeini (Nymphalidae: Heliconiinae). Some butterflies, such as those belonging to the Parnassius simo group, have apparently lost the structure secondarily. The material cost of producing the sphragis is considerable. It is typically offset by production of a smaller spermatophore, thus reducing the amount of male-derived nutrients donated to the female during mating for use in oogenesis and/or somatic maintenance. The sphragis potentially represents one of the clearest examples of mate conflict known. Investigating its biology should yield testable hypotheses to further our understanding of the selective processes at play in an ‘arms race’ between the sexes. This paper provides an overview, which will inform future study.
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