Introduction
Introduced and invading populations generally show low genetic
variability, and a different genetic structure than in their native
range, due to small founder populations, and demographic bottlenecks
(Hufbauer, Bogdanowicz, & Harrison, 2004). Low genetic variability may
in turn influence population level dynamics, persistence, and
evolutionary potential of introduced populations (Fauvergue, Vercken,
Malausa, & Hufbauer, 2012; Szucs, Melbourne, Tuff, & Hufbauer, 2014).
The individuals founding new populations usually bring along various
symbiotic passengers. A common example of such a symbiont is the
α-Proteobacterium Wolbachia pipientis - a maternally inherited
endosymbiotic bacterium that infects over 40% of insect species
(Detcharoen, Arthofer, Schlick-Steiner, & Steiner, 2019).Wolbachia can be intimately involved in the biology of their
hosts, through either manipulating the host reproductive system
(O’Neill, Hoffman, & Werren, 1997), susceptibility to predators,
parasites or pathogens (Fytrou, Schofield, Kraaijeveld, & Hubbard,
2006; Hedges, Brownlie, O’Neill, & Johnson, 2008; Osborne,
Iturbe-Ormaetxe, Brownlie, O’Neill, & Johnson, 2012; van Nouhuys,
Kohonen, & Duplouy, 2016), metabolism (Gruntenko et al., 2017;
Gruntenko et al., 2019), or dispersal capacities (Evans et al., 2009).Wolbachia -mediated costs and benefits have been shown to affect
host population dynamics (Charlat et al., 2009; Duplouy, Hurst, O’Neill,
& Charlat, 2010; Verne, Johnson, Bouchon, & Grandjean, 2012), select
for particular host genotypes (Signor, 2017), or even hamper the
evolution of host traits in infected populations (Martinez et al.,
2016). Consequently, studying spatio-temporal patterns in the penetrance
and prevalence of symbionts in host populations along with the genetic
structure of introduced and original host populations, can provide
crucial insights into how both intentionally and accidentally introduced
species may successfully establish, persist and further disperse across
habitats (Lu, Hulcr, & Sun, 2016).
The Glanville fritillary butterfly, Melitaea cinxia (L.)
(Lepidoptera: Nymphalidae) lives as a classical metapopulation in Åland,
Finland (I. Hanski, Pakkala, Kuussaari, & Lei, 1995). The
(meta)population ecology and dynamics of the butterfly and associated
community of parasitoid species has been under study since the early
90’s (van Nouhuys & Hanski, 2005), revealing, for example, that the
butterfly population dynamics dictates the population sizes of its
associated parasitoids (I. Hanski et al., 2017). In August 1991,
seventy-two families of gregarious M. cinxia caterpillars were
intentionally introduced on the island of Sottunga, on the East side of
the Åland archipelago (Fountain et al., 2018; I. Hanski et al., 2004; I.
Hanski et al., 2017). Through natural parasitism of about a third of the
introduced butterfly larvae, the specialist parasitoid waspHyposoter horticola (Gravenhorst) (Hymenoptera: Ichneumonidae:
Campoplaginae), and its own specialist hyperparasitoid Mesochoruscf. stigmaticus (Hymenoptera: Ichneumonidae: Mesochorinae) (I.
Hanski et al., 2004; G. C. Lei, Vikberg, Nieminen, & Kuussaari, 1997;
Montovan, Couchoux, Jones, Reeve, & van Nouhuys, 2015; Shaw,
Stefanescu, & Van Nouhuys, 2009; van Nouhuys & Ehrnsten, 2004) were
simultaneously accidentally introduced in Sottunga. As they make up the
highest trophic levels of insect communities, parasitoids are extremely
sensitive to the spatio-temporal dynamics and structure of their host
resources (Cronin & Reeve, 2005; Gagic et al., 2012; Gagic et al.,
2011; Kaartinen & Roslin, 2011; Nair, Fountain, Ikonen, Ojanen, & van
Nouhuys, 2016; van Nouhuys, 2005). Nonetheless, despite occasional
strong bottlenecks through local butterfly population crashes (Fountain
et al., 2016; I. Hanski et al., 2004; van Bergen et al., 2020), the
three species have persisted on Sottunga, more than 30km away from the
mainland population, and more than 12km away from any other island
population. In this system, Wolbachia is only known to infect the
parasitoid wasp, H. horticola (Duplouy, Couchoux, Hanski, & van
Nouhuys, 2015). In Åland, the host population infection occurs at an
intermediate and stable rate of about ≈50% across the archipelago
(Duplouy et al., 2015), but the local prevalence of the bacterium
differs between the mainland and neighbouring isolated islands (Duplouy
et al., 2015), and the infection is more often associated to one of the
two previously described mitochondrial haplotypes of the host (Duplouy
et al., 2015). Finally, the infection is costly and increases, by almost
two folds, the susceptibility of infected individuals to the
hyperparasitoid (van Nouhuys et al., 2016), which itself varies in
prevalence and rate of hyperparasitism across local populations in Åland
(Montovan et al., 2015; Nair et al., 2016).
We analysed spatio-temporal variations in both the genetic structure of
the parasitoid host, H. horticola, and the infection rate of the
parasitoid by the endosymbiont Wolbachia on the island of
Sottunga, and four other regions in the Åland islands. We used 14
nuclear microsatellite markers and one mitochondrial marker to genotype
324 wasps, to infer history and outcome of the accidentally introduced
small population, over a 22year period (1992-2013), and screened the
wasps for infection with Wolbachia over the same period. We
investigated (1) whether gene flow occurred after the accidental
introduction of the parasitoid species on the island of Sottunga, and
migrations supported persistence of the neighbouring island populations
despite occasional population crashes, and (2) whether variations in the
local levels of hyperparasitism selected for Wolbachia -infected
or uninfected host genotypes in isolated local populations.