RESEARCH: HYBRID SPECIATION AND MIMICRY IN THE PAPILIO GLAUCUS SPECIES GROUP

The North American butterfly world was pleasantly surprised when Harry Pavulaan and David Wright discovered in 2002 a new species of a very large and colourful tiger swallowtail butterfly. They named it Papilio appalachiensis, the Appalachian tiger swallowtail, which is endemic to the Appalachian Mountains in the eastern United States. Now, it is very rare to find a new species of such a large butterfly, but what made this discovery even more remarkable and exciting was the apparent phenotypic mixture in this species of two other closely related species: the Canadian tiger swallowtail (P. canadensis) and the eastern tiger swallowtail (P. glaucus). The Appalachian tiger swallowtail occurs in the cooler thermal habitat at mid- to high-elevations in the Appalachian Mountains, and has a single generation per year. It also has an uninterrupted yellow band on the forewing underside and rectangular yellow lunules on the hindwing submarginal area. These physiological, life history and morphological features are similar to the Canadian tiger swallowtail. On the other hand, its black female form and female dimorphism, which are related to Batesian mimicry of the toxic pipevine swallowtail (Battus philenor), are similar to that of the eastern tiger swallowtail. Based on this mixed phenotype, Pavulaan and Wright (2002, 2004) speculated that the Appalachian tiger swallowtail was a hybrid species formed from an ancient hybridization event between the Canadian and eastern tiger swallowtails. If true, this would be a very exciting example of hybrid speciation in animals. Hybrid speciation, in which hybridization between two species results in an independent daughter species, is considered very rare in animals. Little is known about how and why hybrid species are formed and maintained. However, it is important to know these things about hybrid speciation because it is a novel way of generating new species from existing variation.

So, in the summer and fall of 2006, Krushnamegh Kunte drove nearly 15,000 miles to sample all the eight tiger swallowtail butterflies throughout most of their ranges in North America, shown below:

Then, beginning from 2009, we started a detailed genetic analysis of the three focal species (appalachiensis, glaucus and canadensis) to test the hypothesis that appalachiensis was a hybrid species. We compared sequences of one mitochondrial and six Z-linked genes in the three species, and found out that appalachiensis is glaucus-like for its mitochondrial gene which cosegregates with the female-specific W chromosome in butterflies, and on which the main gene for mimicry is situated in the eastern tiger swallowtail. On the other hand, it is canadensis-like for the Z-linked genes that are closely linked to pupal diapause that is crucial in its cold themal habitat. Thus, it appears that appalachiensis has inherited most its Z chromosome and cold thermal habitat genes from canadensis and its W chromsome and mimicry from glaucus.

Next, we tested for a genome-wide signature of admixture in appalachiensis using hundreds of nuclear markers known as AFLPs. AFLPs showed that appalachiensis has nearly equal genomic contributions from glaucus and canadensis. Using the sequence and AFLP data, we further estimated that appalachiensis was formed during the last interglacial period in North America, approximately 100,000 years ago, after which it seems to have hybridized very little with the parental species.

Since appalachiensis largely overlaps with glaucus and still remains a distinct species, and given its specific combination of traits from the two parental species that is clearly under selection, it appears that appalachiensis is maintained as a hybrid species due to natural selection for mimicry and traits necessary to survive in a cold thermal habitat. Overall, it represents a telling example of hybrid species that informs us on the dynamics of hybrid speciation in animals.
 

References:

Deshmukh, R., S. Baral, A. Gandhimathi, M. Kuwalekar, and K. Kunte. 2017. Mimicry in butterflies: co-option, and a bag of magnificent developmental genetic tricks. WIREs Developmental Biology, in press.

Arnold, M. L. and K. Kunte. 2017. Adaptive genetic exchange: a tangled history of admixture and evolutionary innovation. Trends in Ecology and Evolution, 32:601–611. PDF file (1.8MB, has colour figures). Recommended by Faculty of 1000 (F1000Prime) (download the recommendation if you do not have a subscription).

Zhang, W., K. Kunte, and M. R. Kronforst. 2013. Genome-wide characterization of adaptation and speciation in tiger swallowtail butterflies using de novo transcriptome assemblies. Genome Biology and Evolution, 5:1233-1245.

Kunte, K., C. Shea, M. L. Aardema, J. M. Scriber, T. E. Juenger, L. E. Gilbert, and M. R. Kronforst. 2011. Sex chromosome mosaicism and hybrid speciation among tiger swallowtail butterflies. PLoS Genetics, 7:e1002274. See the full paper online on the journal website, or its news coverage on the National Science Foundation (NSF, USA) website, the University of Texas at Austin and the College of Natural Sciences websites, or in Harvard Gazette.