Vagabonding female butterflies weigh in on reproductive strategies

August 19, 2020

Many animals respond to unfavourable environmental changes in their habitat by migrating or dispersing to other areas. Seasonally recurring changes in habitat conditions have led to such spectacular annual events as the large mammalian migrations across the African plains, and the monarch butterfly migrations across North America. India has its share of large-scale migrations and dispersals: millions of waterfowl migrate from the northern regions to India and back around winter, and a countless number of insects disperse over long distances as seasons and habitats change. A new study by researchers from the National Centre for Biological Sciences (NCBS), Bengaluru, published today in the Royal Society's journal Biology Letters, shows that such dispersals, when undertaken by butterflies in search of unpredictable resources, selectively burden the egg-carrying females on their long flights. This has implications for the persistence of populations in a changing environment, especially in an ever-fragmenting natural world.

Let us first distinguish between migration and dispersal for our purposes. Migrations are long-range cyclical movements, i.e. when animals move in a specific direction in a specific season between two known destinations. Thus, seasonal movements of waterfowl between Siberia and India are considered migrations. On the other hand, dispersals are movements in which the direction and distance are unpredictable, and they are undertaken when local resources are exhausted. So, dispersals are essentially movements in a random direction in search of new resource patches whose locations are unknown. Considering these differences in the nature of movement, what effects do dispersals versus migrations have on the decisions of animals regarding whether - and how much - to invest in reproduction and flight when moving?

To study these aspects, Vaishali Bhaumik, a PhD student at NCBS and SASTRA University, and her advisor Dr Krushnamegh Kunte, turned to butterflies--their favourite insects. They had observed that caterpillars of the Lemon Emigrant and Mottled Emigrant butterflies (Catopsilia pomona and Catopsilia pyranthe) seasonally strip off nearly all the leaves from their larval host plants. This forces adult butterflies to disperse for uncertain distances in search of new habitat patches where they may be able to find larval host plants with sufficient foliage on which to lay eggs. Emigrants sometimes end up dispersing for hundreds of kilometres before they settle down in a patch to breed.

The research team compared the flight morphology and reproductive status of these two species of Emigrant with two other sets of butterflies: one containing milkweed butterflies that migrate annually across southern India in response to the Indian monsoon, and another containing close relatives of Emigrants that do not migrate or disperse long distances at all in India, but mostly breed where they are born.

They discovered that female milkweed butterflies that migrate annually in a predictable manner do so in a state of reproductive diapause; i.e., they completely halt reproductive activity and are therefore not burdened with eggs during the long migratory flights, investing all their energies in movement instead. On the other hand, female Emigrants - the long-distance dispersers - fly in a state of full reproductive maturity, i.e., they carry a heavy load of eggs on their flights. By contrast, males of the species always travel light, whether they are migrating, dispersing, or not. Thus, dispersals selectively burden the flight of egg-carrying females.

The study suggests that this stark contrast in reproductive strategies of migrating versus dispersing butterflies stems from differences in the predictability of habitat patches and larval host plants. The annual migrations of milkweed butterflies occur between known habitat patches, so there is some certainty about finding the right habitat patch at a predictable time in relation to the monsoon. So, a reproductive diapause, which takes time to break, and subsequently delayed courting, mating and egg-laying, seems to be a feasible option for migrating milkweed butterflies.

On the other hand, seasonal leaf flushing makes larval hosts a prime resource that Emigrant caterpillars must exploit while it lasts.

These plants occur in randomly available patches, depending on whether other butterflies (and their caterpillars) have already been there. This uncertainty and intense competition for short-lived larval host plant resources mean that female Emigrants have to be ready to lay eggs as soon as they find a suitable host plant patch.

Therefore, a reproductive diapause during dispersal is perhaps not a feasible option for them. This might explain why they disperse while being burdened by eggs that are ready to be laid. Thus, the ability to disperse in a reproductively ready mode comes at the cost of a more expensive flight.

These findings suggest that some species - and their females in particular - may be more vulnerable to the vagaries of long-distance flights to uncertain destinations. This ought to be a vexing problem for a large number of species because of increasingly fragmented and sometimes vanishing habitat patches in a large unsuitable matrix, in which their colonization potential may be compromised.

"Such research findings are a first step towards conservation efforts taken up by the forest department especially for lesser known species such as butterflies," said Shri Ajai Misra, IFS, Principal Chief Conservator of Forests (Wildlife) & Chief Wildlife Warden, Karnataka Forest Department, which has supported a string of projects by Dr. Kunte's lab. "The Karnataka Forest Department is utilizing such studies in understanding habitat corridors being used for dispersal/migration by different species so that biodiversity in larger landscapes can be preserved."

Ms. Bhaumik ponders upon what this might mean for the evolution of female traits and reproductive strategies. "Might females have evolved larger flight muscles to be able to fly long distances with their heavy egg loads? Do older and younger females in a large population vary in their abilities to produce more eggs versus disperse further in an uncertain world? Could this lead to alternative reproductive strategies such as 'stay home and breed' versus 'travel far, die trying, but prosper sometimes if lucky'?"

Such thinking opens up a whole new world of looking at butterflies and other critters in fascinating ways. Dr. Kunte and his students cherish these opportunities. He chimed in, "We were fortunate to wonder about how males and females differ in their morphology, reproductive strategies and other biology, and what these differences might tell us about the natural world at large. This has opened up wonderful avenues to start asking interesting questions about the evolution of sexual dimorphism, functional diversity, and biodiversity at large." Dr. Kunte's students have equipped themselves to address such queries with a vast morphometric dataset of hundreds of butterfly species across multiple continents.

What secrets of nature will such large datasets reveal? We will find out!
Citation of the paper:

Bhaumik, V., and K. Kunte. 2020. Dispersal and migration have contrasting effects on butterfly flight morphology and reproduction. Biology Letters, 16:20200393.


Additional reference:

Bhaumik, V., and K. Kunte. 2018. Female butterflies modulate investment in reproduction and flight in response to monsoon-driven migrations. Oikos, 127:285-296.


National Centre for Biological Sciences

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