Mimetic host shifts in an endangered social parasite of ants

Jeremy A Thomas,Karsten Schönrogge,Marcin Sielezniew,Graham W Elmes,Anna Stankiewicz-Fiedurek,Josef Settele,David J Simcox

doi:10.1098/rspb.2012.2336

Abstract

An emerging problem in conservation is whether listed morpho-species with broad distributions, yet specialized lifestyles, consist of more than one cryptic species or functionally distinct forms that have different ecological requirements. We describe extreme regional divergence within an iconic endangered butterfly, whose socially parasitic young stages use non-visual, non-tactile cues to infiltrate and supplant the brood in ant societies. Although indistinguishable morphologically or when using current mitochondrial and nuclear sequence-, or microsatellite data, Maculinea rebeli from Spain and southeast Poland exploit different Myrmica ant species and experience 100 per cent mortality with each other's hosts. This reflects major differences in the hydrocarbons synthesized from each region by the larvae, which so closely mimic the recognition profiles of their respective hosts that nurse ants afford each parasite a social status above that of their own kin larvae. The two host ants occupy separate niches within grassland; thus, conservation management must differ in each region. Similar cryptic differentiation may be common, yet equally hard to detect, among the approximately 10 000 unstudied morpho-species of social parasite that are estimated to exist, many of which are Red Data Book listed.

Highlights

To set meaningful priorities in conservation and for practical remedies to succeed, it is vital to ascertain whether the threatened morpho-species named in Red Data lists are likely to consist of more than one cryptic species [1,2] or functionally distinct genotypes
We studied the regional divergence that appeared to exist within the endangered cuckoo butterfly Maculinea rebeli (Hirschke), which was itself indistinguishable from a close relative, Maculinea alcon (Denis & Schiffermuller), in recent molecular studies [20,21]
We made three types of non-parametric analysis of the rank order in which chosen items were retrieved, within or between treatments: Kruskal–Wallis to establish whether ants rescued items randomly or selectively; Wilcoxon to test for changes in the order of selected items after Ma. rebeli had lived for 7 days with the ants compared with the initial 3 h; Mann–Whitney to test for differences in the order in which ant brood or butterfly caterpillars were selected within each of the eight combinations of ants and butterflies shown in figure 2

Summary

Introduction

To set meaningful priorities in conservation and for practical remedies to succeed, it is vital to ascertain whether the threatened morpho-species named in Red Data lists are likely to consist of more than one cryptic species [1,2] or functionally distinct genotypes. Six recognized morpho-species are iconic flagship insects, long identified as global conservation priorities [15,16,17], that possess attributes associated with cryptic speciation [2], including socially parasitic young stages that use non-visual, non-tactile cues, including chemical and acoustical mimicry, to infiltrate and exploit ant societies [15,16,17,18,19]. Larvae infiltrate Myrmica ant colonies in their final instar, where they live for 11– 23 months and acquire more than 98 per cent of their ultimate biomass (see the electronic supplementary material, figure S1) [9] They achieve this transition by abandoning their host plant and secreting simple cocktails of hydrocarbons that resemble the chemical signatures of Myrmica grubs sufficiently well to trick foraging workers of any Myrmica species to ‘rescue’ the mimic and carry it into the underground brood chambers [9,18]. A total of 123 Ma. rebeli larvae from Poland and 97 from Spain were introduced in rspb.royalsocietypublishing.org Proc R Soc B 280: 20122336 rspb.royalsocietypublishing.org Proc R Soc B 280: 20122336

Poland

Results

Findings

Discussion