Strong dispersal in a parasitoid wasp overwhelms habitat fragmentation and host population dynamics

Abstract

The population dynamics of a parasite depend on species traits, host dynamics and the environment. Those dynamics are reflected in the genetic structure of the population. Habitat fragmentation has a greater impact on parasites than on their hosts because resource distribution is increasingly fragmented for species at higher trophic levels. This could lead to either more or less genetic structure than the host, depending on the relative dispersal rates of species. We examined the spatial genetic structure of the parasitoid wasp Hyposoter horticola, and how it was influenced by dispersal, host population dynamics and habitat fragmentation. The host, the Glanville fritillary butterfly, lives as a metapopulation in a fragmented landscape in the Åland Islands, Finland. We collected wasps throughout the 50 by 70 km archipelago and determined the genetic diversity, spatial population structure and genetic differentiation using 14 neutral DNA microsatellite loci. We compared the genetic structure of the wasp with that of the host butterfly using published genetic data collected over the shared landscape. Using maternity assignment, we also identified full-siblings among the sampled parasitoids to estimate the dispersal range of individual females. We found that because the parasitoid is dispersive, it has low genetic structure, is not very sensitive to habitat fragmentation and has less spatial genetic structure than its butterfly host. The wasp is sensitive to regional rather than local host dynamics, and there is a geographic mosaic landscape for antagonistic co-evolution of host resistance and parasite virulence.

Spatial and temporal genetic structure at the fourth trophic level in a fragmented landscape

“…This movement results in a weak spatial genetic structure. The contrast between species is further supported by lack of IBD in the hyperparasitoid (electronic supplementary material, figure S5), strong IBD in the parasitoid C. melitaearum [11], and comparatively weaker IBD in the parasitoid H. horticola [28].…”

“…Figure 3. Distribution in the landscape of the offspring of the parasitoid Hyposoter horticola (black) (data from [28]) and the hyperparasitoid Mesochorus cf. stigmaticus (grey) indicated by the proportion of sibling pairs presented as (a) a hierarchy of localities and (b) distance apart in metres (distance between siblings from the same habitat patch was not measured).…”

“…The structure we found for the butterfly is qualitatively the same as found for samples collected in 2002, using four microsatellite markers and 10 neutral SNPs [51] suggesting that the butterfly has had a relatively stable degree of population structure over time. The primary parasitoid, occupying the next trophic level, also shows a spatial genetic structure at the level of SINs, but the genetic differentiation is weak (F ST ¼ 0.07, [28]), with fewer spatially defined genetic clusters (K ¼ 15) than the host butterfly. Using data from the same year as were used for the parasitoid (2009-2010), the hyperparasitoid had just K ¼ 4 genetic clusters and little spatial pattern in the observed genetic structure.…”

“…The number ranged from 22 to 175 individuals per year, depending on host butterfly population size, the rate of parasitism, and rearing conditions. For comparison, we calculated the population structure of the parasitoid H. horticola using 407 samples (for details, see [28]) and the host butterfly M. cinxia using samples (n ¼ 421) collected across Å land in 2010.…”

Wolbachiaincreases the susceptibility of a parasitoid wasp to hyperparasitism

“…The study area, Åland, is a Finnish archipelago in the Baltic Sea, where the butterfly lives as a classical metapopulation in a 50 by 70 km fragmented landscape (Hanski, 2011). The wasp occupies the entire host metapopulation (Couchoux et al, 2016). About half of the wasp population is infected by a unique Wolbachia strain, wHho (Duplouy et al, 2015).…”