Anne Andersen:
Spatiotemporal and conservation genetics of the large blue butterfly (Maculinea arion)

Date: 31-07-2018    Supervisor: David R. Nash

Symbioses are long-term interactions among different species. They sort on a gradient from mutualistic (beneficial to both species) to parasitic (one species benefits at the expense of the other). Butterflies that form symbioses with ants are rare, found only among the butterfly families Riodinidae and Lycaenidae. The main focus of this thesis is the large blue butterfly (Maculinea arion L. 1758, Lycaenidae), a social parasite of ants. However, one chapter explores the symbiosis between the Irenea metalmark (Thisbe irenea Stoll 1780, Riodinidae) and its host ant: a symbiosis that can be placed at the other end of the gradient, although is not always mutualistic. In this thesis, I focus on the spatiotemporal genetics of the threatened Palearctic large blue butterfly. The main objectives were to shed light on the genetic consequences of the species’ peculiar life history, and how habitat fragmentation and land-use affects the population genetic structure and genetic diversity in this species.

Anthropogenic land-use changes impact the size, quality and connectivity of species’ habitats, subsequently affecting population genetic structure, dispersal and level of genetic diversity in species. The large blue butterfly has experienced severe population declines and extinctions during the last century throughout most of its European range. The species’ has a peculiar lifecycle requiring both a specific food plant and host ant, consequently the species is rare and patchily distributed.

In the first chapter, I investigate the population genetic consequences of the species’ peculiar life history. I used 14 microsatellite loci to study the population genetic structure and diversity over eight generations in six populations in two separate regions. I found that the level of genetic diversity was constant despite all populations having experienced recent genetic bottlenecks. Populations only separated by two generations were genetically differentiated. This differentiation was attributable to a high allelic turnover rather than nestedness, which would be expected if populations had lost genetic diversity. I suggest that associative overdominance, a mechanism only present in small populations due to heterozygote advantage, maintains the level of genetic diversity in these populations. The signs of recent genetic bottlenecks, however, are attributable to the species’ lifecycle, where only a small subset of individuals survives to adulthood, and these individuals are likely to be more related than random due to strong selection pressures from the host ant.

In the second chapter, I focus on the consequences of habitat fragmentation on the population genetic structure and level of genetic diversity in different landscapes across the species’ range. The study was based on fourteen microsatellite markers and included 520 individuals from fourteen areas in six regions. I found that populations in all regions had unique genetic diversity. Populations in the eastern and southern part of the species’ range had higher genetic diversity than the other populations. Populations in more continuous landscapes had higher migration rates, subsequently lower genetic differentiation, than did populations living in more fragmented landscapes. Within areas, the level of genetic diversity and differentiation correlated with the habitat size and distance to nearest habitat patch, respectively. Similarly, the number of migrants was inversely correlated with the mean distance among habitat patches within an area, while the genetic diversity was correlated with the amount of semi-natural land in the area. In conclusion, for effective management of this species, it is important to distinguish between recently derived genetic structure and an equilibrium state. The low levels of gene flow in Western Europe appear to be a consequence of landscape features rather than species’ biology.

In the third study, I investigate the mutualistic symbiosis between the Irenea metalmark and its host ant through field behavioural experiments and chemical analyses of the butterfly caterpillars and ants cuticular hydrocarbons. I found that the ant protects all development stages of the butterfly caterpillar, despite not receiving rewards from early instars. Furthermore, I found overlap between the cuticular hydrocarbons of caterpillars in different development stages. Thus, the ants might associate the odour of early instars with rewards from later instars. However, greater understanding of the ant’s ability to perceive cues from caterpillars is necessary to confirm this hypothesis.

This thesis contributes to the understanding of how the population genetic structure and genetic diversity is affected by both habitat fragmentation and land-use, and the species’ extraordinary lifecycle. The results have implications for the conservation of this threatened species in a time of anthropogenic climate change and land-use change affecting the distribution and diversity of species.