The Build-Up of Population Genetic Divergence along the Speciation Continuum during a Recent Adaptive Radiation of Rhagoletis Flies

Abstract

New species form through the evolution of genetic barriers to gene flow between previously interbreeding populations. The understanding of how speciation proceeds is hampered by our inability to follow cases of incipient speciation through time. Comparative approaches examining different diverging taxa may offer limited inferences, unless they fulfill criteria that make the comparisons relevant. Here, we test for those criteria in a recent adaptive radiation of the Rhagoletis pomonella species group (RPSG) hypothesized to have diverged in sympatry via adaptation to different host fruits. We use a large-scale population genetic survey of 1568 flies across 33 populations to: (1) detect on-going hybridization, (2) determine whether the RPSG is derived from the same proximate ancestor, and (3) examine patterns of clustering and differentiation among sympatric populations. We find that divergence of each in-group RPSG taxon is occurring under current gene flow, that the derived members are nested within the large pool of genetic variation present in hawthorn-infesting populations of R. pomonella, and that sympatric population pairs differ markedly in their degree of genotypic clustering and differentiation across loci. We conclude that the RPSG provides a particularly robust opportunity to make direct comparisons to test hypotheses about how ecological speciation proceeds despite on-going gene flow.

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

“…A population of these flies shifted from infesting the fruit of native downy hawthorn ( Crataegus mollis ) to introduced apple ( Malus pumila ) during the mid‐19th century (Bush, 1966; Walsh, 1861) and divergent adaptation to these two host plants in the subsequent ~170 generations has led to substantial but incomplete reproductive isolation between the two host‐associated populations of R. pomonella (Feder et al, 1988, 1994; Michel et al, 2010). The resulting consistent allele frequency differentiation between sympatric apple‐ and hawthorn‐infesting population pairs support the position of the derived apple fly at the hypothesized “host race” stage of ecological speciation in phytophagous insects (Berlocher & Feder, 2002; Drès & Mallet, 2002; Powell et al, 2013, 2022). The primary axes of divergent host plant adaptation driving reproductive isolation in this system are chemosensory adaptation to host fruit volatiles, which are the major cues for mating aggregation (Linn et al, 2003) and diapause‐mediated life history timing corresponding to differences in fruiting phenology of the host plants (Feder et al, 2010; Filchak et al, 2000).…”

“…The resulting consistent allele frequency differentiation between sympatric apple-and hawthorn-infesting population pairs support the position of the derived apple fly at the hypothesized "host race" stage of ecological speciation in phytophagous insects (Berlocher & Feder, 2002;Drès & Mallet, 2002;Powell et al, 2013Powell et al, , 2022. The primary axes of divergent host plant adaptation driving reproductive isolation in this system are chemosensory adaptation to host fruit volatiles, which are the major cues for mating aggregation (Linn et al, 2003) and diapause-mediated life history timing corresponding to differences in fruiting phenology of the host plants (Feder et al, 2010;Filchak et al, 2000).…”

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

“…Taken together, our results highlight the difficulty of predicting the ecological and evolutionary ramifications of climate change. If responses to climate warming are highly varied and complex, even among populations that have been diverging for only ~170 years, still share all their genomic variation (Doellman et al, 2019;Powell et al, 2022), and occur in the same habitat and location, we have a long way to go in understanding which species and communities may be most vulnerable to altered seasonality. Our results further suggest that these outcomes may be governed by nuanced effects of differences in thermal reaction norms for life-history traits acting across organisms' life cycles, and identifying maladaptive tipping points in these systems should be a goal of future empirical work on insects and climate change.…”

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

“…The combination of temporal isolation and prezygotic reproductive isolation due to divergent chemosensory adaptation (Linn et al 2003; Dambroski et al 2005) limits on-going hybridization between apple and hawthorn flies at sympatric sites to 4-6% (Feder et al 1994). Genetic differentiation in this system is based on consistent frequency differences in shared alleles rather than fixed variants between host races (Michel et al 2010, Powell et al 2013, 2022, Meyers et al 2020).…”