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

Abstract

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.

Secondary reversion to sexual monomorphism associated with tissue-specific loss of doublesex expression

“…This linkage is a logical consequence of the mainly cell-autonomous control of sexual differentiation in insects: with rare exceptions, cells that transcribe dsx have the potential to differentiate in sex-specific ways, while those that lack dsx expression do not (Camara et al, 2008; Hopkins and Kopp, 2021; Kopp, 2012; Ledón-Rettig et al, 2017). It will be interesting to see whether the pattern of gains and losses of dsx expression extends to other models where sex-specific traits have been both gained and lost – such as beetle horns (Emlen et al, 2005; Moczek et al, 2006), Lepidopteran androconia (Prakash and Monteiro, 2020; Simmons et al, 2012; Valencia-Montoya et al, 2021), or Batesian mimicry in swallowtail butterflies (Kunte, 2009; Palmer and Kronforst, 2020).…”

Genomics‐based higher classification of the species‐rich hairstreaks (Lepidoptera: Lycaenidae: Eumaeini)

“…The tribe Eumaeini (Lepidoptera: Lycaenidae) is biologically notable for being a rapidly diversifying clade. With an estimated age of approximately 30 million years, it is one of the youngest recognized tribes of butterflies (Espeland et al, 2018; Valencia‐Montoya et al, 2021). With about 1200 New World and 100+ Palearctic species (Robbins, 2004a; Weidenhoffer, Bozano, & Churkin, 2004), it is also one of the most species‐rich with 7%–8% of the world's diurnal butterfly species (Lamas, 2008).…”

“…Many proposed lineages based on morphology were poorly characterized (Robbins, 2004a), and those that were readily recognized, such as the Atlides Section and the Lamprospilus Section (later named Calycopidina), were based on homoplastic characters (Duarte & Robbins, 2010; Martins, Duarte, & Robbins, 2019a). A molecular analysis based upon 187 eumaeines recognized eight lineages, but no taxonomic changes were proposed (Valencia‐Montoya et al, 2021). Congruence between morphological and molecular groupings was limited.…”

“…Eumaeines are evolutionarily notable for a variety of male secondary sexual organs that have been associated with diversification (Valencia‐Montoya et al, 2021). For example, males of the Neotropical Arcas cypria (Geyer) have scent pads, scent patches, scent pouches and abdominal brush organs (Martins, Duarte, & Robbins, 2019b; Robbins, Martins, Busby, & Duarte, 2012).…”

“…For example, males of the Neotropical Arcas cypria (Geyer) have scent pads, scent patches, scent pouches and abdominal brush organs (Martins, Duarte, & Robbins, 2019b; Robbins, Martins, Busby, & Duarte, 2012). Over 90% of eumaeine species possess at least one male secondary sexual organ (Valencia‐Montoya et al, 2021). The seven male secondary sexual organs in one clade ( Atlides Section) were gained or lost within the lineage, often multiple times (Martins et al, 2019b).…”