Non-parallel morphological divergence following colonization of a new host plant

Abstract

Adaptation to new ecological niches is known to spur population diversification and may lead to speciation if gene flow is ceased. While adaptation to the same ecological niche is expected to be parallel, it is more difficult to predict whether selection against maladaptive hybridization in secondary sympatry results in parallel divergence also in traits that are not directly related to the ecological niches. Such parallelisms in response to selection for reproductive isolation can be identified through estimating parallelism in reproductive character displacement across different zones of secondary contact. Here, we use a host shift in the phytophagous peacock fly Tephritis conura, with both host races represented in two geographically separate areas East and West of the Baltic Sea to investigate convergence in morphological adaptations. We asked (i) if there are consistent morphological adaptations to a host plant shift and (ii) if the response to secondary sympatry with the alternate host race is parallel across contact zones. We found surprisingly low and variable, albeit significant, divergence between host races. Only one trait, the length of the female ovipositor, which serves an important function in the interaction with the hosts, was consistently different between host races. Instead, co-existence with the other host race significantly affected the degree of morphological divergence, but the divergence was largely driven by different traits in different contact zones. Thus, local stochastic fixation or reinforcement could generate trait divergence, and additional evidence is needed to conclude whether divergence is locally adaptive.

Colonization of a novel host plant reduces phenotypic variation

“…We collected thistle buds infested by T. conura during the pupal stage at all these locations (Fig. S1) and allowed adults to eclose in a common laboratory environment as described in Nilsson et al (2022). The sampling scheme enables us to examine to what extent patterns of phenotypic variance are explained by host plant adaptations and by regional sympatry with the other host race.…”

“…To produce variables to include in later analyses we took the first six principal components which explained 68% of the total phenotypic variation. The melanised area of the wing was measured through an automated script developed in MATLAB (Matlab 2017) as in Nilsson et al (2022). All subsequent statistical analyses were performed in R version 3.6.1 (R Core Team 2019).…”

“…Patterns of trait divergence allowed us to formulate hypotheses about past or current patterns of selection on different traits. The ovipositor is shorter in the derived host race (Diegisser et al 2007; Nilsson et al 2022), and is thus likely either to be or to have been under directional selection to match the bud size of the derived host plant. The directional selection on ovipositor length in the derived host race may have depleted the variation in ovipositor length, and of the available combinations of ovipositor length and other traits within the fly populations.…”

“…Interestingly, there is evidence of phenotypic adaptation to the specific host plants, most clearly in the length of the ovipositors. Flies infesting C. oleraceum have shorter ovipositors than flies infesting C. heterophyllum (Diegisser et al 2007; Nilsson et al 2022), matching the smaller bud size of the plant (Romstock-Volkl 1997). Moreover, there is empirical evidence for strongly reduced survival on the alternative host plant (Diegisser et al 2008), suggesting strong host plant-mediated selection.…”

“…First, for traits that differ between the ancestral and derived host race, we expect historical and potentially current directional selection in the derived host race. Specifically, selection on the ovipositor to match the bud size of the derived host plant (Romstock-Volkl 1997) likely caused directional selection in the derived host race which has a shorter ovipositor length compared to the ancestral host race (Diegisser et al 2007; Nilsson et al 2022). This selection may have altered the structure of the phenotypic variance covariance matrix ( P ) in the derived host race in T. conura .…”