Divergence before the host shift? Prezygotic reproductive isolation among three varieties of a specialist fly on a single host plant

Abstract

1. Although divergence via host-plant shifting is a common theme in the speciation of some phytophagous insects, it is not clear whether host shifts are typically initiators of speciation or if they instead contribute to divergence events already in progress. While host shifts appear to be generally associated with speciation events for flies in the genus Strauzia, three sympatric varieties of the sunflower fly [Strauzia longipennis (Wiedemann)] co-occur on the same host plant in the Midwestern United States and may have evolved reproductive barriers without a host shift.2. The strength of two prezygotic reproductive barriers was compared among the three S. longipennis varieties: one barrier that is often associated with divergent ecological selection (allochronic isolation), and another that is more likely to be independent of ecological selection (pre-copulatory sexual isolation). The presence and relative strength of each barrier between fly varieties were evaluated using microsatellites, no choice mating experiments, studies of allochronic isolation, and field collection data.3. Evidence for both allochronic isolation and pre-copulatory sexual isolation was detected between the three varieties of S. longipennis. The measure of isolation calculated for each barrier between the three varieties was lower than measures calculated between different species of Strauzia found on different hosts, suggesting that subsequent host shifts may increase the degree of reproductive isolation. For Strauzia and other specialist insects, some reproductive isolation may evolve prior to, and indeed may facilitate, host shifts.

Host shifting and host sharing in a genus of specialist flies diversifying alongside their sunflower hosts

“…As with the flies associated with H. grosseserratus, the three Strauzia species that feed on pith of H. tuberosus are not one another's closest relatives (Figure 2), such that the most parsimonious explanation for the origin of their host sharing is multiple independent shifts onto the same host plant. While previous work using mitochondrial data and microsatellites hypothesized that the H. tuberosus-associated flies might have resulted from several recent divergence events during periods of isolation in glacial refugia (Hippee et al 2016), this was based on the assumption from taxonomic work that the H. tuberosus flies were three partially isolated, but otherwise closely related "varieties" of S. longipennis (Loew 1873;Foote et al 1993). The inclusion of other Strauzia species in the current work reveals that the H. tuberosus-associated flies are actually not one another's closest relatives, and that they represent distinct, already-isolated lineages that converged upon the same plant.…”

“…However, decades of accumulated evidence suggest that the sawtooth sunflower (Helianthus grosseserratus) and Jerusalem artichoke (H. tuberosus) are each host to multiple Strauzia species. Either two or three fly species are associated with H. grosseserratus (Lisowski 1985;Steyskal 1986;Stoltzfus 1988), while H. tuberosus hosts three genetically differentiated lineages that have variably been referred to as varieties or species, depending on the author (Stoltzfus 1988;Forbes et al 2013;Hippee et al 2016). Evaluating how multiple Strauzia species have come to coexist on their respective plants promises exciting new insights into the origins and maintenance of insect diversity.…”

“…Axen et al (2010) made some initial progress, identifying two haplotype groups within the S. longipennis complex, each closely associated with a particular thoracic striping patternthough the association between haplotype and morphology was imperfect. Later, Forbes et al (2013) and Hippee et al (2016) used AFLP and microsatellite markers, respectively, to demonstrate that the Strauzia flies reared from Helianthus tuberosus include three genetically distinct groupings. The microsatellite-based analyses in particular showed a 1:1 correlation between each genetic cluster and a particular combination of thoracic stripes and wing patterns (Hippee et al 2016).…”

“…Later, Forbes et al (2013) and Hippee et al (2016) used AFLP and microsatellite markers, respectively, to demonstrate that the Strauzia flies reared from Helianthus tuberosus include three genetically distinct groupings. The microsatellite-based analyses in particular showed a 1:1 correlation between each genetic cluster and a particular combination of thoracic stripes and wing patterns (Hippee et al 2016). This work strongly suggests that the H. tuberosus-associated S. longipennis complex consists of at least three different species, but their relationships to one another, and to flies with similar morphologies on other host plants, remains uncertain.…”

“…First, fly species sharing a single host may all share a recent common ancestor that used the same plant host, and which diversified without host shifts, perhaps during periods of geographic isolation (e.g., in refuges during glacial periods; Rand 1948). In this "no host shift" scenario (proposed in Hippee et al 2016), the nowreproductively isolated sister species would later have become sympatric once the temporarily fragmented geographic distribution of their host plant fused back into a contiguous range. An alternative "host shift" scenario is that flies originating on different hosts converged upon single plant species via multiple host shifting events.…”