Mimicry in Papilio polytes: Papilio polytes, otherwise known as the Common Mormon butterfly, ranges widely from Sri Lanka and India to Indo-China, S. Japan, the Philippines and Sunda Islands in SE Asia. Its caterpillars feed on a variety of Rutaceae plants (Citrus and allied genera, including lemon and orange plants) and the butterfly is palatable to its predators such as birds. Various female forms of this species derive protection from such predators with their resemblance to distantly related, chemically protected (toxic) Pachliopta butterflies, which experienced birds avoid eating. This type of resemblance is called Batesian mimicry, which is restricted in P. polytes to females, and the toxic species they resemble are called "models". Throughout its range, and in numerous subspecific variations, P. polytes has a single non-mimetic male form, with which cyrus, a male-like non-mimetic female form, co-occurs (see the figure). Most populations also have up to two female forms that mimic locally available Pachliopta species. The female-limited mimetic polymorphism reaches its apex in Sri Lanka and peninsular India where, in the subspecies P. p. romulus, three female forms fly together: form cyrus is male-like and non-mimetic, form polytes (=stichius) mimics Pachliopta aristolochiae and Pachliopta pandiyana (Pachliopta jophon in Sri Lanka), and form romulus mimics Pachliopta hector. Note that the two Pachliopta models have wing color patterns very dissimilar to each other, and the P. polytes mimetic female forms also have non-overlapping wing color patterns that very closely mimic the wing patterns of their models. The discrete nature of mimetic polymorphism is crucial: closely-matching mimetic patterns are selectively advantageous but any patterns intermediate between the model phenotypes may be selectively disadvantageous since predators may not recognize them as protective, and so consume them. This has apparently shaped the genetic architecture of mimicry (see below).
Inheritance of the female forms: Inheritance of the female forms in P. polytes is well-known from the work of Clarke & Sheppard from the 1970s. The mimicry genes are autosomal. Expression of the mimetic patterns is strictly female-limited and sex-limitation does not break down in intra- or even interspecific hybrids. At least three genes control the mimetic phenotype, and individuals in South Asian populations are typically heterozygous for them. However, there is a clear dominance hierarchy between the female forms and the dominance is complete, as follows: romulus > polytes > cyrus. Thus, matings between females of any form and males of any ancestry can produce non-mimetic as well as all mimetic female forms, depending on the genetic constitution of the parents.
In view of this suite of interesting biological details, we are studying the molecular genetic basis of female-limited mimicry in P. polytes. Eventually, we would like to understand the genetics of wing patterning in this species and also extend this to other Papilio swallowtails, which show an astounding variation in wing color patterning, mimicry and sexual dimorphism. With this diverse group of butterflies, we are addressing questions such as: (a) Are the same genes involved in mimetic resemblance and have similar genetic changes taken place to produce similar wing pattern elements in different species groups during their independent evolution of mimicry? (b) Is the genetic architecture of mimicry similar in these species groups? In other words, are genes situated in similar places in the genome, are similar number of genes involved in mimicry, and are they similarly expressed or regulated?
The long-term goal of our lab's research is to study the genetic basis of sexual dimorphism and phenotypic polymorphism, and to test the theory of the evolution of supergenes. A supergene is a tight cluster of genes within which there is little recombination. The tight clustering produces sets of alleles of different genes in a supergene that together produce alternative phenotypes. Because there is very little recombination between the genes, intermediate phenotypes are almost never produced. A supergene is suspected to be involved in mimicry in Papilio polytes, in which the last property of supergenes – lack of recombination and subsequent phenotypic intermediates – is critical. Intermediates between the discrete mimetic female forms would not be recognized as mimetic by predators and be eaten. The evolution of supergenes would prevent this mortality. By comparative approach we would eventually be able to test whether mimicry supergenes have evolved in P. polytes and other Batesian mimics.
References:
Deshmukh, R., D. Lakhe, and K. Kunte. 2020. Tissue-specific developmental regulation and isoform usage underlie the role of doublesex in sex differentiation and mimicry in Papilio swallowtails. Royal Society Open Science, 7:200792. PDF file (1.3MB).
Baral, S., Gandhimathi A., R. Deshmukh, and K. Kunte. 2019. Genetic architecture and sex-specific selection govern modular, male-biased evolution of doublesex. Science Advances, 5:eaau3753. PDF file (5.5MB).
Deshmukh, R., S. Baral, A. Gandhimathi, M. Kuwalekar, and K. Kunte. 2018. Mimicry in butterflies: co-option and a bag of magnificent developmental genetic tricks. WIREs Developmental Biology, 7:e291. PDF file (8.5MB, has colour figures).
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).
Kunte, K., W. Zhang, A. Tenger-Trolander, D. H. Palmer, A. Martin, R. D. Reed, S. P. Mullen, and M. R. Kronforst. 2014. doublesex is a mimicry supergene. Nature, 507:229–232. PDF file (1.2MB). Recommended by Faculty of 1000 (F1000Prime) (download the recommendation if you do not have a subscription). Read more about the story on this webpage. See popular science coverage of this paper in Nature, Nature India, Science, NCBS News, The Scientist, National Geographic's Phenomena blog, Mongabay, New York Times, The Hindu, and ScienceDaily.
