Sämi Schär:
The evolution of exploitation strategies by myrmecophiles

Date: 03-02-2014    Supervisor: David Richard Nash

Myrmecophiles are animals which have evolved to live in the nests of ants. This life history strategy appears in animals as different as insects, spiders, snails, crustaceans and even snakes. Myrmecophiles are very speciose with estimates of up to 100'000 species, which raises the question why this strategy has evolved so frequently and is maintained by natural selection. The type of association between Myrmecophiles and ants ranges from mutualistic through to parasitic. These types of symbioses can also be found between and within species of ants. Ant associations can therefore be broadly categorized into three major types: (1) Host associated ant lineages that evolved from subpopulations of their own species (intraspecific social parasitism). (2) Ant species which evolved in the way mentioned in (1) but in the mean time became good species (Social parasites according to Emery's rule) and (3) Species - whether ants or other animals - that evolved ant association de novo from ancestors which did not interact with the present ant associates. In this PhD thesis I have investigated ant associations of the 1st and the 3rd type and the evolutionary consequences of mutualism and parasitism for both the host ants and their associates. In the first chapter I found clear evidence for the parasitic nature of ant microgynes in the species Myrmica rubra from the virulence resulting from their presence. Additionally I found that the presence of microgynes goes hand in hand with reduced longevity of the macrogyne host queens in the same nests. This implies that microgynes either reduce host queen life span, or more likely prefer exploitation of colonies containing disproportionally many old host queens. In a second chapter I found that the abundance of entomopathogens was significantly reduced in ant nests (Myrmica rubra and M. ruginodis) compared to their environment, suggesting that myrmecophiles living in nests of those ants may benefit immunologically from this strategy. Further I discovered that specific pathogens like the common entomopathogenic fungus Metarhizium brunneum were less abundant inside than outside ant nests (M. rubra) as well. This fungus can kill ant associated lycaenid larvae, justifying the assumption that these benefit from the entomopathogen poor environment of ant nests. This could explain why natural selection may act in favour of this strategy. In the third chapter I investigated the genetic consequences of ant association types in a butterfly family (Lycaenidae) which contains variation in type and degree of ant association, using mitochondrial COI DNA sequences. I found that ecological specialization on different host ants (obligate ant association) most likely does not enhance diversification in the Lycaenidae, as has been suggested earlier, and is therefore probably not the most promising explanation for their outstanding diversity. Genetic diversity is highest in lycaenids which have only facultative and non-specific associations with ants (generalists). This could mean that the ability of the Lycaenidae to colonize "enemy free space" (the large proportion of terrestrial habitats that are dominated by ants) is more likely to explain the extraordinary diversity of the Lycaenidae rather than their ecological specialization, assuming that diversity can result from ecological success. Finally, the fourth chapter sheds light on genetic diversity of populations and lineage ages of six butterfly (Lycaenidae) species in relation to geography and especially latitude and longitude. I found strong variation in intraspecific diversity of COI between related butterfly species. Furthermore their genetic structure shows the signature of the ice ages, apparent in latitudinal gradients of genetic diversity and the inferred age of endemic lineages. I hope that the results of this study can directly be applied in optimization of local butterfly conservation strategies in Denmark and elsewhere. The thesis ends with conclusions and an outlook of how the results from this project could be directly applied or be followed up in future studies.