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Diel behavior in moths and butterflies: a synthesis of data illuminates the evolution of temporal activity

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Abstract

Lepidoptera (butterflies and moths) are one of the most taxonomically diverse insect orders with nearly 160,000 described species. They have been studied extensively for centuries and are found on nearly all continents and in many environments. It is often assumed that adult butterflies are strictly diurnal and adult moths are strictly nocturnal, but there are many exceptions. Despite the broad interest in butterflies and moths, a comprehensive review of diel (day-night) activity has not been conducted. Here, we synthesize existing data on diel activity in Lepidoptera, trace its evolutionary history on a phylogeny, and show where gaps lie in our knowledge. Diurnality was likely the ancestral condition in Lepidoptera, the ancestral heteroneuran was likely nocturnal, and more than 40 transitions to diurnality subsequently occurred. Using species diversity estimates across the order, we predict that roughly 75-85% of Lepidoptera are nocturnal. We also define the three frequently used terms for activity in animals (diurnal, nocturnal, crepuscular), and show that literature on the activity of micro-moths is significantly lacking. Ecological factors leading to nocturnality/diurnality is a compelling area of research and should be the focus of future studies.

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Acknowledgements

We thank James K. Adams, Evan Braswell, Charles V. Covell Jr., Jurate De Prins, James E. Hayden, Chris Johns, Ian Kitching, Shigeki Kobayashi, Sei Maruyama, Deborah Matthews, Erik van Nieukerken, Richard Peigler, Rodolphe Rougerie, Andrei Sourakov, Emmanuel Toussaint, Andrew Warren, Andreas Zwick, and an anonymous reviewer for insightful comments. Photographs in Fig. 1 were taken by Patrick Clement, Gail Hampshire, Donald Hobern, Pavel Kirilov, Carla Kishinami, Jürgen Magelsdorf, Ronnie Pitman, Lary Reeves, Line Sabroe, Alan Schmierer, Ken-ichi Ueda, Alexey Yakovlev, and Mark Yokoyama.

Funding

This study was funded by NSF DEB grant numbers 1541500 and 1557007 to AYK, NSF IOS-1121739 and IOS-1121807 to AYK and JRB, and NSF PRFB-1612862 to CAH.

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Authors and Affiliations

  1. Florida Museum of Natural History, University of Florida, Gainesville, FL, 32611, USA

    Akito Y. Kawahara, David Plotkin, Chris A. Hamilton, Harlan Gough, Ryan St Laurent, Hannah L. Owens & Nicholas T. Homziak

  2. Department of Entomology and Nematology, University of Florida, Gainesville, FL, 32611, USA

    Akito Y. Kawahara, David Plotkin & Nicholas T. Homziak

  3. Department of Biology, University of Florida, Gainesville, FL, 32611, USA

    Akito Y. Kawahara, Harlan Gough & Ryan St Laurent

  4. Department of Biological Sciences, Boise State University, Boise, ID, 83725, USA

    Jesse R. Barber

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Electronic supplementary material

Fig. S1

Ancestral state reconstruction of diel activity in adult Lepidoptera, based on a make.simmap analysis in ‘phytools’. The phylogeny was inferred using a ‘nt123_partitioned’ Regier et al. (2013) dataset with a backbone constraint composed of Kawahara and Breinholt (2014) and Bazinet et al. (2017). Nodes correspond to the posterior probabilities of a state with over 10,000 simulations. Colors: black = nocturnal, blue = crepuscular, orange = diurnal, gray = all. Branches are colored according to their character state and where along the branch transitions likely occurred. (PDF 440 kb)

Fig. S2

Ancestral state reconstruction of diel activity in adult Lepidoptera, based on a make.simmap analysis in ‘phytools’. The phylogeny was inferred using the ‘nt123’ Regier et al. (2013) dataset with a backbone constraint composed of Kawahara and Breinholt (2014) and Bazinet et al. (2017). Nodes correspond to the posterior probabilities of a state with over 10,000 simulations. Colors: black = nocturnal, blue = crepuscular, orange = diurnal, gray = all. Branches are colored according to their character state and where along the branch transitions likely occurred. (PDF 456 kb)

Fig. S3

Ancestral state reconstruction of diel activity in adult Lepidoptera, based on a make.simmap analysis in ‘phytools’. The phylogeny was inferred using the ‘nt123_degen1’ Regier et al. (2013) dataset with a backbone constraint composed of Kawahara and Breinholt (2014) and Bazinet et al. (2017). Nodes correspond to the posterior probabilities of a state with over 10,000 simulations. Colors: black = nocturnal, blue = crepuscular, orange = diurnal, gray = all. Branches are colored according to their character state and where along the branch transitions likely occurred. (PDF 444 kb)

Fig. S4

Character states mapped for each tip of the phylogeny, using a ‘nt123_partitioned’ Regier et al. (2013) dataset and the Kawahara and Breinholt (2014) and Bazinet et al. (2017) chimaera topological constraint. Colors: black = nocturnal, blue = crepuscular, orange = diurnal, gray = all. (PDF 23 kb)

Table S1

Compilation of diel activity times of adult Lepidoptera. Taxonomic information in Columns A-F is taken directly from the Regier et al. (2013) dataset, and in a few instances does not reflect more recent taxonomic changes. Column G contains the species’ code names used as tip labels on the phylogeny in Fig. S1. In situations where diel activity was unavailable for a particular species, the citations listed in Column H correspond to diel activity for a higher-level taxon containing that species, as indicated in Column J. (XLSX 90 kb)

Table S2

Attributions for Lepidoptera images used in Fig. 1. (XLSX 42 kb)

Table S3

Character state matrix used in ancestral state reconstructions. (TXT 19 kb)

Table S4

Diel probabilities of selected higher monophyletic lepidopteran groups. Values are probabilities generated in SIMMAP on the “nt123_partitioned” dataset. (XLSX 48 kb)

ESM 1

Supp. Tree 1. Kawahara and Breinholt (2014) and Bazinet et al. (2017) backbone tree used as a topological constraint in the present study. (TRE 1023 bytes)

ESM 2

Supp. Tree 2. ML tree file using the original Regier et al. (2013) ‘nt123_partitioned’ dataset with topological constraints mentioned in the methods. The dataset was partitioned by site. (TRE 32 kb)

ESM 3

Supp. Tree 3. ML tree file built from the original Regier et al. (2013) ‘nt123’ dataset with topological constraints mentioned in the methods. (TRE 32 kb)

ESM 4

Supp. Tree 4. ML tree file built from the original Regier et al. (2013) ‘nt123_degen1’ dataset with topological constraints mentioned in the methods. (TRE 32 kb)

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Kawahara, A.Y., Plotkin, D., Hamilton, C.A. et al. Diel behavior in moths and butterflies: a synthesis of data illuminates the evolution of temporal activity. Org Divers Evol 18, 13–27 (2018). https://doi.org/10.1007/s13127-017-0350-6

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