High Rate of Protein Coding Sequence Evolution and Species Diversification in the Lycaenids

Abstract

Understanding the variations in the rate of molecular evolution among lineages may provide clues on the processes that molded extant biodiversity. Here, we report the high rate of molecular evolution in Lycaenidae and Riodinidae compared to other families of butterflies (Papilionoidea). We assembled a phylogeny of butterflies using eight molecular markers and comprising 4,891 species. We found that the rate of molecular evolution is higher in Lycaenidae and Riodinidae compared to the other families, but only the nuclear protein coding sequence Wingless showed a marked difference, while Elongation factor 1-alpha showed a more moderate difference. In contrast, Cytochrome Oxidase subunit 1 showed no difference between Lyacenidae and Riodinidae, and other butterflies. In parallel, we calculated the rates of diversification in all subfamilies of the Papilionoidea using the method-of-moments estimator for stem-group ages, which does not require a fully solved phylogeny for the target clades. We found that the Lycaeninae lineage, from the Lycaenidae family had the highest rate of diversification among all lineages. Among the life-history traits that could explain differences in molecular evolution and diversification rate, lycaenids display mutualistic or antagonistic interactions with ants, a higher level of host plant specialization and reduced dispersal abilities compared to other butterfly families. Since the current study is limited by a unique contrast, the relationship with traits cannot be evaluated statistically. Future studies should measure myrmecophily and dispersal abilities quantitatively across a more detailed phylogeny of lycaenids to test for an association between shifts in the strength of mutualism, rates of molecular evolution and the diversification of lineages.

Rapid radiation of ant parasitic butterflies during the Miocene aridification of Africa

“…The few butterfly species feeding on resources other than plants (i.e., aphytophagous lineages) are found primarily in Lycaenidae and Riodinidae, which have independently evolved high degrees of ant association (Espeland et al, 2018 ; Pierce et al, 2002 ). Symbiotic ant association is thought to have promoted diversification in the Lycaenidae as a whole (Pellissier et al, 2017 ; Pierce et al, 2002 ; Schär et al, 2018 ). However, even though entomophagy has evolved many times independently in Lycaenidae, this strategy generally appears to be an evolutionary dead‐end since it has rarely led to diversification (Cottrell, 1984 ; Pierce, 1995 ; Pierce et al, 2002 ; Schär et al, 2018 ), with Lepidochrysops as the striking exception.…”

The Bear Giant-Skipper genome suggests genetic adaptations to living inside yucca roots

“…Next, the position of Calycopis (family Lycaenidae) in the tree is less strongly supported (96%) than other nodes, which possibly results from its elevated evolutionary rate: C. cecrops forms a long branch compared to other species included in the tree (Fig. 6) (Cong, Shen et al 2016;Cong, Shen et al 2017a;Pellissier, Kostikova et al 2017). However, this placement of Lycaenidae as a sister to Nymphalidae (represented by Danaus, Heliconius and Melitaea) in our tree agrees with morphology and other DNA evidence (Mutanen, Wahlberg et al 2010;Heikkila, Kaila et al 2012;Cong, Shen et al 2016;Cong, Shen et al 2017c).…”

Molecular taxonomy of Tomares hairstreaks (Lepidoptera, Lycaenidae, Theclinae)

“…Over the last decade, lycaenid butterflies have been a popular model group in studies of hybridization (Mallet et al 2011;Gillespie et al 2013;Nice et al 2013;Sakamoto and Yago 2017), sympatric and cryptic speciation (Dincă et al 2011;Vodă et al 2015;Lukhtanov et al 2015;Busby et al 2017;Bereczki et al 2018), population genomics (Gompert et al 2014;Vanden Broeck et al 2017;Chaturvedi et al 2018), chromosome evolution (Lukhtanov and Dantchenko 2017), ecological specialization (Downey and Nice 2013; Schär et al 2018) and conservation genetics (Sielezniew et al 2012;Frye and Robbins 2015;Takeuchi et al 2015;Koubínová et al 2017;Roitman et al 2017;Matthews et al 2018). Part of this popularity maybe due to the fact that lycaenids have the highest rate of protein-coding sequence evolution among butterflies (Pellissier et al 2017). Nevertheless, lycaenid taxonomy is still riddled with cases of uncertainty.…”