New research sheds fresh light on the evolutionary genetics of sex-limited polymorphic mimicry in swallowtail butterflies

by Rahul Kumar

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Mimicry is an evolutionary strategy where an organism imitates another species to gain a survival advantage. Mimicry is the product of co-evolution. Co-evolution involves reciprocal evolutionary changes between two or more interacting species. Being part of an evolutionary ancient phylum, arthropods have diversified extensively. This diversity is attributed to the evolution of innumerable survival strategies which make arthropods the most successful animals on earth. Interestingly, mimicry is one such adaptive feature. There are various kinds of mimicry out of which Batesian mimicry is the one where a harmless species resembles an undesirable or hazardous or distasteful species to get protection from predators. Papilio polytes, a common swallowtail butterfly, is an excellent model to study Batesian mimicry. P. polytes exhibits sex-limited Batesian mimicry where females are mimetic and males are non-mimetic. In some populations, non-mimetic female forms also exist. Also, mimetic females mimic different model species across different habitats. Such mimicry, where individuals of the same species mimic different models across different habitats, is called polymorphic mimicry.

Recently, a group of Indian scientists led by Dr Krushnamegh Kunte from Biodiversity Lab, National Centre for Biological Sciences, Bengaluru, has deciphered the mechanism behind the existence and maintenance of different canalized morphs (different mimetic and non-mimetic forms) in the populations of P. polytes butterflies using specimens collected through extensive sampling across mainland Asia (particularly South Asia) and islands like Philippines and Java. Canalization is an evolutionary process through which an organism’s phenotype is stabilized against genetic or environmental variations, ensuring consistent developmental outcomes. Stability of these morphs is attributed to a large inversion of the chromosomal region containing a conserved gene doublesex (dsx) which is considered a mimicry supergene. Through a series of analysis involving both molecular and in silico tools, it has been found that these butterflies evolved about 9.8 million years ago with P. protenor as the basal taxa where both males and females are non-mimetic and monomorphic and there is no inversion of the aforementioned chromosomal segment. Both female-limited mimicry and dsx inversion found in all mimetic forms of P. polytes are derived states and were absent in the ancestral form. Whole genome sequencing, 

Genome-wide Association Studies (GWAS), genotype-phenotype mapping, developmental expression studies and allelic characterisation reveal that different forms of P. polytes share dsx alleles as well the associated inversion breakpoints. Crossing pure-breeding lines of different forms show that dominance hierarchy among the alleles governing wing patterns exist between various forms. The mimetic form romulus, which evolved later in due course of evolution, have alleles dominant over another mimetic form polytes which is older than form romulus. Likewise, form polytes exhibits allelic dominance over non-mimetic form cyrus. Interbreeding between various mimetic and non-mimetic forms does not break this allelic dominance hierarchy and the resulting appearance of sex-limited mimicry. It makes non-mimetic phenotypes universally recessive and mimetic phenotypes universally dominant. This step-wise evolution of female forms is a case of what is called Haldane’s sieve (named after British geneticist J. B. S. Haldane). Haldane’s sieve refers to an evolutionary phenomenon where dominant beneficial alleles have a higher chance of becoming fixed in a population than recessive ones. These novel dominant alleles (which are  initially rare) are subjected to directional selection and selective sweeps for fixation. In this study also, it was found that dsx alleles have signatures of selective sweeps and episodic positive selection (=directional selection acting intermittently) across different mimetic forms as well as other mimetic species of Papilio butterfly leading to their rapid evolution. 

Although integrity of dsx alleles is protected by inversion and lack of recombination across the inverted segment, novel mimetic forms have been reported to exist in nature with intermediate phenotypes between the form romulus and form polytes (romulus like forewings and polytes like hindwings). Breeding experiments using this intermediate form yielded fertile and genetically stable offspring. Occurrence of this novel intermediate form is attributed to rare exon swaps in the aforementioned genetic locus.

This study offers valuable insights into the evolutionary genetics of both mimetic and non-mimetic forms of P. polytes as well as other mimetic Papilio species. Present work makes us appreciate how complex intricate molecular mechanisms shape the evolution of earth’s remarkable diversity of life forms. Each animal holds innumerable secrets and evolution has all the answers!

For more details, please refer:

Riddhi Deshmukh, Saurav Baral, Athulya Girish Kizhakke, Muktai Kuwalekar and Krushnamegh Kunte (2024). Evolution of novel mimicry polymorphisms through Haldane’s sieve and rare recombination. eLife13:RP101346. https://doi.org/10.7554/eLife.101346.1  

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About the author:

Dr Rahul Kumar is one of the associate editors of “Indian Entomologist.” He is currently working as an Assistant Professor and Head of the Department of Zoology at Sheodeni Sao College (Magadh University), Kaler-824127, India. His ongoing research primarily addresses the behavioural, evolutionary, and taxonomic aspects of insects and spiders. Additionally, he has worked on molecular biology (eukaryotic gene regulation) at JNU, New Delhi; nanotechnology (nano-therapeutics and diagnostics) at AIIMS, New Delhi; science education (activity-based teaching-learning) at NCERT, New Delhi and insect taxonomy (micro-moths) at ICAR-IARI, New Delhi as a research fellow. He can be contacted at rahuldayanand33@gmail.com. 

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