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

Fabien L. Condamine, Benoit Nabholz, Anne Laure Clamens, Julian R. Dupuis, Felix A.H. Sperling

Research output: Contribution to journalArticlepeer-review

25 Scopus citations

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.

Original languageEnglish
Pages (from-to)460-480
Number of pages21
JournalSystematic Entomology
Volume43
Issue number3
DOIs
StatePublished - Jul 2018

Bibliographical note

Funding Information:
We are grateful to Sophie Dang, Troy Locke and Corey Davis at the Molecular Biology Service Unit of the University of Alberta for their help, assistance and advice on the next-generation sequencing. We appreciate the helpful reviews of the manuscript by Niklas Wahlberg and an anonymous reviewer. Financial support was provided by a Marie Curie International Outgoing Fellowship (project 627684 BIOMME) to FLC, and an NSERC Discovery Grant to FAHS.

Publisher Copyright:
© 2018 The Royal Entomological Society

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Insect Science

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