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

Robert K. Robbins, Qian Cong, Jing Zhang, Jinhui Shen, Robert C. Busby, Christophe Faynel, Marcelo Duarte, Ananda R.P. Martins, Carlos Prieto, Gerardo Lamas, Nick V. Grishin

Research output: Contribution to journalArticlepeer-review

Abstract

We propose a higher classification of the lycaenid hairstreak tribe Eumaeini – one of the youngest and most species-rich butterfly tribes – based on autosome, Lepidopteran Z sex chromosome and mitochondrial protein-coding genes. The subtribe Neolycaenina Korb is a synonym of Callophryidina Tutt and subtribe Tmolusina Bálint is a synonym of Strephonotina K. Johnson, Austin, Le Crom, & Salazar. Proposed names are Rhammina Prieto & Busby, new subtribe; Timaetina Busby & Prieto, new subtribe; Atlidina Martins & Duarte, new subtribe; Evenina Faynel & Grishin, new subtribe; Jantheclina Robbins & Faynel, new subtribe; Paiwarriina Lamas & Robbins, new subtribe; Cupatheclina Lamas & Grishin, new subtribe; Parrhasiina Busby & Robbins, new subtribe; Ipideclina Martins & Grishin, new subtribe; and Trichonidina Duarte & Faynel, new subtribe. Phylogenetic results from the autosome and Z sex chromosome analyses are similar. Future analyses of datasets with hundreds of terminal taxa may be more practical time-wise by focussing on the smaller number of sex chromosome sequences (2.6% of nuclear protein-coding sequences). The phylogenetic classification and biological summaries for each subtribe suggest that a variety of factors affected Eumaeini diversification. About a dozen kinds of male secondary sexual organs with frequent evolutionary gains and losses occur in Atlidina, Evenina and Jantheclina (141 species combined). Females have been shown to use these organs to discriminate between conspecific and nonconspecific males, facilitating sympatry among close relatives. Eumaeina, Rhammina and Timaetina (140 species combined) are overwhelmingly montane with some evidence for a higher incidence of sympatric diversification. Seven Neotropical lineages in five subtribes invaded the temperate parts of the Nearctic Region with a diversification increase in the Callophryidina (262 species). North American Satyrium and Callophrys then invaded the Palearctic at least once each, with a major species-richness increase in Satyrium. The evolution of litter-feeding detritivores within Calycopidina (172 species) resulted in an increase in diversification rate compared with its flower-feeding sister lineage. Atlidina, Strephonotina, Parrhasiina and Strymonina (562 species combined) each contain a mixture of genera that specialize on one or two caterpillar food plant families and genera that are polyphagous. These would be appropriate subtribes to assess how the breadth of caterpillar food plants and the frequency of host shifts affected diversification.

Original languageEnglish
JournalSystematic Entomology
DOIs
StateAccepted/In press - 2022
Externally publishedYes

Bibliographical note

Funding Information:
We thank Naomi Pierce and Wendy Valencia‐Montoya for discussions of eumaeine evolution. We are grateful to Greg Ballmer, Vitor Becker, Matthew Cock, Phil DeVries, Winnie Hallwachs, Dan Janzen, the late Roy Kendall, Olaf Mielke, Deb Murray and many others for sharing vouchers of reared species and related information. Thanks to Niklas Wahlberg and Naomi Pierce for checking an identification in the Chazot publication. We thank William Beck, David Geale and Andrew Neild for the images in Figure 4A, 4H, 4I , 10A, 10B, respectively. We are especially grateful to the curators of the museum collections noted for allowing us access to their collections. Robert K. Robbins acknowledges support from an ADS core proposal grant from the National Museum of Natural History. Nick V. Grishin acknowledges support from the NIH (GM127390) and the Welch Foundation (I‐1505). Marcelo Duarte acknowledges support from FAPESP (grants 2002/13898‐0, 2003/13985‐3 and 2016/50384‐8), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (PROTAX II – grant 440597/2015‐3), Conselho Nacional de Desenvolvimento Científico e Tecnológico (grants 305905/2012‐0, 311083/2015‐3 and 312190/2018‐2) and Universidade de São Paulo (Projeto 1, Pró‐Reitoria de Pesquisa).

Funding Information:
Conselho Nacional de Desenvolvimento Científico e Tecnológico, Grant/Award Numbers: 305905/2012‐0, 311083/2015‐3, 312190/2018‐2; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Grant/Award Number: 440597/2015‐3; FAPESP, Grant/Award Numbers: 2002/13898‐0, 2003/13985‐3, 2016/50384‐8; United State National Institutes of Health (NIH), Grant/Award Number: GM127390; NMNH ADS core; Welch Foundation, Grant/Award Number: I‐1505 Funding information

Publisher Copyright:
© 2022 Royal Entomological Society. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.

Keywords

  • diversification
  • food plant specialization
  • male secondary sexual organs
  • polyphagy
  • Theclinae
  • Z sex chromosome

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