Polymorphic growth in larvae of the butterflyMaculinea rebeli, a social parasite ofMyrmicaant colonies

Abstract

Caterpillars of Maculinea rebeli have two growth strategies for living underground as social parasites of Myrmica ant colonies. Laboratory experiments and ¢eld data show that 25% of caterpillars live ten months with ants before pupating, whereas 75% grow slowly, parasitizing their hosts for 22 months. Both types of caterpillar form apparently identical similar-sized pupae. This may be the ¢rst description in the animal kingdom of polymorphic growth rates spanning di¡erent years within the same population, yet without resulting (as in salmonid ¢sh) in two morphologically distinct adult types with obvious di¡erences in behaviour. We suggest that a balanced polymorphism has evolved in M. rebeli growth rates, representing the most e¤cient way of exploiting the limited, yet steady, daily supply of food available to cuckoo-feeding parasites of long-lived ant societies. Bet-hedging bene¢ts would also accrue to adult butter£ies producing a mixture of annual and biennial o¡spring. Despite ergonomic and other bene¢ts, partial biennialism is unlikely to evolve unless slow-growing individuals have enhanced survival and can remain attached to their mobile hosts. We show that caterpillars become so closely protected by, and integrated with, their host colonies that slow growers experience no greater mortality over two years than fast growers over one, and are transported in preference to the ants' own larvae when the host colony moves nest site.

Polymorphic growth rates in myrmecophilous insects

“…To compare the new Maculinea and Microdon data to those of M. rebeli further, we used the body weight measurements of two M. rebeli caterpillars and 12 pupae collected from nests of Myrmica schencki Emery in 1999 in the Pyrenees in addition to the data published by Thomas et al (1998b).…”

“…Cultures were maintained for a few weeks after pupation ceased, then most experiments were terminated because small cultures of Myrmica deteriorate after 12 months in the laboratory . Any caterpillars which were alive and healthy two weeks after pupation ceased were assumed to be biennials as demonstrated for M. rebeli (Thomas et al 1998b). This was also con¢rmed for M. alcon using a small number of cultures which were maintained for a second year.…”

“…The close mimicry of ant larvae by M. rebeli also promotes the persistence of the host colony until the parasites complete their larval development. Thomas et al (1998b) predicted that a few other myrmecophiles may have evolved this unusual annual^biennial polymorphism in response to ergonomic and social conditions in host ant nests. However, we thought this would be con¢ned to other cuckoo-feeding social parasites such as Maculinea alcon (Dennis & Schi¡.…”

“…Thus, insight into the dynamics and evolution of ant^parasite associations also increases our understanding of whole community dynamics. Thomas et al (1998b) recently demonstrated that a single cohort of larvae drawn from a population of the myrmecophilous butter£y Maculinea rebeli (Hirschke) contains ca. 25% of individuals which develop and eclose within one year and 75% which develop over two years, irrespective of food supply, ambient temperature and other biotic or abiotic factors.…”

“…In other species, the extended juvenile stage has been interpreted as a way of minimizing local extinction by catastrophic events (`bet hedging') (Hanski 1988;Hanski & Stahls 1990;Thomas et al 1998b) or unusually short growing conditions. Thomas et al (1998b) hypothesized that biennialism evolved in M. rebeli as an ergonomic adaptation which results in nearly double the number of eggs from an individual mother surviving to adulthood, although, once evolved, the mixture of annual and biennial morphs would have additional bet-hedging advantages.…”