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.

Understanding the evolutionary potential of populations —evolvability— is key to predicting their ability to cope with novel environments. Despite growing evidence that evolvability determines the tempo and mode of adaptation, it remains unclear how adaptations to novel environments influence evolvability in turn. Here we address the interplay between adaptation and evolvability in the peacock fly Tephritis conura, which recently underwent an adaptive change in the length of female ovipositor following a host shift. By comparing evolvability in various morphological traits including female ovipositor length between ancestral and derived host races, we found that evolvability is decreased in females of the derived host race compared to the ancestral host race. We found a correlation between evolvability and divergence between populations in both sexes, indicating that the overall pattern of evolvability has not been disrupted by the host shift despite the reduction in females of the derived host race. Exploration of the pattern of phenotypic integration further revealed that the ovipositor length constitutes a module that is separated from other measured traits. These results suggest that adaptation to novel environments can affect evolvability, and that modularity helps minimizing detrimental effects that adaptations may cause to other correlated traits.

Adaptation to novel ecological niches is known to be rapid. However, how ecological divergence translates into reproductive isolation remains a consequential question in speciation research. It is still unclear how coupling of ecological divergence loci and reproductive isolation loci occurs at the genomic level, ultimately enabling the formation of persistent species. Here, we investigate the genomic underpinning colonization of a new niche and formation of two host races in Tephritis conura peacock flies that persist in sympatry. To uncover the genomic differences underlying host plant adaptation, we take advantage of two independent sympatric zones, where host plant specialists using the thistle species Cirsium heterophyllum and C. oleraceum co-occur, and address what regions of the genome that diverge between the host races in a parallel fashion. Using Population Branch Statistics, dxy and BayPass we identify 2996 and 3107 outlier regions associated with host use among western and eastern Baltic populations, respectively, with 82% overlap. The majority of outliers are located within putative inversions, adding to the growing body of evidence that structural changes to the genome are important for adaptations to persist in face of gene flow. Potentially, the high contents of repetitive elements could have given rise to the inversions, but this remains to be tested. The outlier regions were enriched for genes involved in e.g. metabolism and morphogenesis, potentially due to the selection for processing different metabolites, and changes in size and ovipositor length respectively. In conclusion, this study suggests that structural changes in the genome, and divergence in independent ecological functions may facilitate the formation of persistent host races in face of gene flow.