Simulated climate change causes asymmetric responses in insect life history timing potentially disrupting a classic ecological speciation system

Abstract

Climate change may alter phenology within populations with cascading consequences for community interactions and on-going evolutionary processes. Here, we measured the response to climate change in two sympatric, recently diverged (~170 years) populations of Rhagoletis pomonella flies specialized on different host fruits (hawthorn and apple) and their parasitoid wasp communities. We tested whether warmer temperatures affect dormancy regulation and its consequences for synchrony across trophic levels and allochronic isolation between divergent populations. Under warmer temperatures, both fly populations developed earlier. However, warming significantly increased the proportion of maladaptive pre-winter development in apple, but not hawthorn, flies. Parasitoid phenology was less affected, potentially generating ecological asynchrony. Observed shifts in fly phenology under warming may decrease allochronic isolation, potentially limiting on-going divergence. Our findings of complex sensitivity of life-history timing to changing temperatures predict that coming decades may see multifaceted ecological and evolutionary changes in temporal specialist communities.

The role of sexual isolation during rapid ecological divergence: Evidence for a new dimension of isolation in Rhagoletis pomonella

“…In Rhagoletis pomonella , CHCs are a putative mating signal, and CHC profiles differ between apple and hawthorn flies (Hood et al, 2021). Moreover, recent research suggests a possible connection between diapause life history timing, which is known to be heavily influenced by temperature (i.e., Feder et al, 2010; Lackey et al, 2022) and brain development in R. pomonella (Kharva et al, 2022). Kharva et al (2022) show that faster post‐winter development is associated with changes in pupal brain chemistry which persist in the adult stages.…”

“…Regardless of the underlying mechanisms, how future warming will affect the overall dynamics of this and other systems with on‐going speciation will ultimately depend on the multifaceted influence of temperature acting across the life cycle and the potential individual or synergistic effects on different phenotypes involved in reproductive isolation. For instance, changes to the symmetry of sexual isolation may act on top of decreased temporal isolation due disrupted diapause (Lackey et al, 2022), which in turn will be superimposed on potential changes to host plant phenology.…”

“…, from existing data. Data for temporal isolation were calculated for 1284 Apple and 1037 Hawthorn flies reared under control temperatures from the same experiment from which flies were used for sexual isolation mating trials described in this study (Lackey et al, 2022). For habitat isolation, we used data from fruit volatile preferences in flight tunnels (Linn et al, 2003).…”

“…Individual strengths of isolating barriers estimate the proportion of gene flow limited by each barrier if acting alone. We compared total sexual isolation from Control rearing conditions calculated in this study to measures of temporal isolation from our data on eclosion timing (Lackey et al, 2022) and habitat isolation from previously published work on attraction preference to host fruit volatiles (Linn et al, 2003) (Figure 2a). Temporal isolation was moderate in strength (RI = 0.44, 95% CI: 0.31-0.56).…”

“…Third, we tested whether rearing fly pupae under temperature regimes that mimic climate change predictions in the next 50–100 years affected mating interactions with consequences for the strength of sexual isolation, and thus, the potential for speciation. Lastly, we compared the strength of sexual isolation to measures of temporal and habitat isolation from existing data (Lackey et al, 2022; Linn et al, 2003) to place the strength of sexual isolation in the context of other prezygotic barriers linked to divergent adaptation to different host plants.…”