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Contributed by Daniel H. Janzen, January 16, 2017 (sent for review December 12, 2016; reviewed by May R. Berenbaum and John Shuey)
Significance
Thirteen years of mitochondrial DNA barcoding of 15,000+ species of Lepidoptera and their parasitoids living in Area de Conservación Guanacaste, northwestern Costa Rica, indicate several thousand cases where barcodes combined with ecology suggest unrecognized cryptic species, substantially increasing species counts. Here, we show that the slightly different barcodes of three extremely similar parapatric–sympatric species of butterflies covary not only with ecology and subtle morphological traits but also with nuclear genomes—a finding that we predict will be commonplace and a method that we predict will be widely used. The barcodes of the century-old type specimens of Udranomia kikkawai from Venezuela reveal that this name applies to one of the three Costa Rican cryptic species; the others we describe as new.
Abstract
DNA sequencing brings another dimension to exploration of biodiversity, and large-scale mitochondrial DNA cytochrome oxidase I barcoding has exposed many potential new cryptic species. Here, we add complete nuclear genome sequencing to DNA barcoding, ecological distribution, natural history, and subtleties of adult color pattern and size to show that a widespread neotropical skipper butterfly known as Udranomia kikkawai (Weeks) comprises three different species in Costa Rica. Full-length barcodes obtained from all three century-old Venezuelan syntypes of U. kikkawai show that it is a rainforest species occurring from Costa Rica to Brazil. The two new species are Udranomia sallydaleyae Burns, a dry forest denizen occurring from Costa Rica to Mexico, and Udranomia tomdaleyi Burns, which occupies the junction between the rainforest and dry forest and currently is known only from Costa Rica. Whereas the three species are cryptic, differing but slightly in appearance, their complete nuclear genomes totaling 15 million aligned positions reveal significant differences consistent with their 0.00065-Mbp (million base pair) mitochondrial barcodes and their ecological diversification. DNA barcoding of tropical insects reared by a massive inventory suggests that the presence of cryptic species is a widespread phenomenon and that further studies will substantially increase current estimates of insect species richness.
Footnotes
- ↵1To whom correspondence should be addressed. Email: djanzen{at}sas.upenn.edu.
Author contributions: D.H.J., J.M.B., W.H., and N.V.G. designed research; D.H.J., J.M.B., Q.C., W.H., T.D., R.M., M.H., P.D.N.H., and N.V.G. performed research; D.H.J., J.M.B., Q.C., W.H., R.M., and N.V.G. analyzed data; D.H.J., J.M.B., Q.C., W.H., and N.V.G. wrote the paper.
Reviewers: M.R.B., University of Illinois at Urbana–Champaign; and J.S., The Nature Conservancy.
The authors declare no conflict of interest.
Data deposition: The barcode sequences reported in this paper have been deposited in the GenBank database (accession nos. KY421070, KY421071, and KY421072).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1621504114/-/DCSupplemental.
Nuclear genomes distinguish cryptic species
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