Mitochondrial phylogenomics, the origin of swallowtail butterflies, and the impact of the number of clocks in Bayesian molecular dating

Abstract

Swallowtail butterflies (Lepidoptera: Papilionidae) have been instrumental in understanding many foundational concepts in biology; despite this, a resolved and robust phylogeny of the group has been a major impediment to elucidating patterns and processes of their ecological and evolutionary history. This study presents a mitogenomic, time‐calibrated phylogeny for all swallowtail genera. A shotgun sequencing approach was performed to obtain 32 complete mitogenomes that were added to available butterfly mitogenomes, resulting in a dataset including 142 butterfly taxa (and four outgroups) representing all butterfly families. Phylogenetic analyses were carried out under maximum likelihood (ML) and Bayesian inferences (BIs) with alternative partitioning strategies and the mixture (CAT) model. To test competing hypotheses about the systematics of Papilionidae, such as the enigmatic position of Baronia brevicornis or the status of the tribe Teinopalpini, we estimated the marginal likelihood of alternative topologies and computed Bayes factors. Estimates of divergence times were assessed using a Bayesian relaxed‐clock approach calibrated with six fossils while testing for the number of clocks. The results recovered a well‐resolved and supported phylogeny confirming that Baroniinae is sister to Parnassiinae + Papilioninae, both recovered as monophyletic. It also laid the foundations for classification at tribe and genus level, suggesting that the tribe Teinopalpini only contains the genus Teinopalpus (Meandrusa being sister to Papilio). The number of molecular clocks in dating analyses had a significant impact on divergence times. A single clock recovered an origin of butterflies in the Cretaceous (98, 66–188 Ma) and also for swallowtails (85, 55–163 Ma), while partitioning the clocks yielded an origin of Papilionoidea in the very Late Cretaceous (71, 64–86 Ma), and all butterfly families originated in the aftermath of the Cretaceous–Paleogene extinction. These results challenge previous studies suggesting that butterflies appeared in the Early Cretaceous, 110 Ma, concurrently with the rise of angiosperms.

Aristolochiaceae‐ and Asteraceae‐feeding by larvae of Papilio xuthus L. (Lepidoptera: Papilionidae) in Japan: A review

“…Recently, Condamine et al . () noted “within Papilioninae, our results support earlier morphological results (Munroe & Ehrlich ; Munroe ) by recognizing four monophyletic and well‐supported tribes: Leptocircini, Teinopalpini, Papilionini and Troidini. We further found that Leptocircini is the sister clade to all other Papilioninae, and that Teinopalpini is sister to Papilionini plus Troidini.…”

“…; Condamine et al . ). Speculation that Aristolochiaceae‐feeding represents the ancestral condition within Parnassiinae + Papilioninae was rejected by Miller () and Weintraub () based on cladistic analyses.…”

“…; Condamine et al . ) and on chemical and genetic factors determining host preferences and host shifts (e.g. Berenbaum & Feeny ; Ozaki et al .…”

“…Numerous studies have been made on their speciation, polymorphism, mimicry, sexual selection, host relations, physiology, anatomy and historical biogeography (e.g. Simonsen et al 2011;Condamine et al 2018) and on chemical and genetic factors determining host preferences and host shifts (e.g. Berenbaum & Feeny 2008;Ozaki et al 2011). In Japan, Shirôzu (1955) assessed Forbes' (1932) suggestion that Aristolochiaceae, Magnoliaceae, Lauraceae and Annonaceae were primitive host families for Papilionidae, with which proposition he agreed after minor modifications to current views on papilionid phylogeny.…”

“…Thereafter, various cladistic studies indicated that Parnassius and Troides belong to wholly separate clades, with Papilio being more closely related to Troides than to Parnassius (e.g. Hancock 1983;Miller 1987a;Tyler et al 1994;Parsons 1996;Morinaka et al 1999;Braby et al 2005;Condamine et al 2018). Speculation that Aristolochiaceae-feeding represents the ancestral condition within Parnassiinae + Papilioninae was rejected by Miller (1987b) and Weintraub (1995) based on cladistic analyses.…”