Sequential divergence and the multiplicative origin of community diversity

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 112; no. 44; pp. E5980 - E5989
• Main Authors: Hood, Glen R., Forbes, Andrew A., Powell, Thomas H. Q., Egan, Scott P., Hamerlinck, Gabriela, Smith, James J., Feder, Jeffrey L.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 03.11.2015; National Acad Sciences
• Series: PNAS Plus
• Subjects: Animals; Biodiversity; Biological Sciences; Braconidae; Diptera; DNA, Mitochondrial - genetics; Genetics; Genotype & phenotype; Hymenoptera; Insects; Microsatellite Repeats - genetics; Molecular Sequence Data; PNAS Plus; Rhagoletis pomonella; Tephritidae; Wasps - classification; Wasps - genetics; Wasps - physiology; Rhagoletis; parasitoid; ecological speciation; tritrophic interactions; host plant adaptation
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1424717112

Phenotypic and genetic variation in one species can influence the composition of interacting organisms within communities and across ecosystems. As a result, the divergence of one species may not be an isolated process, as the origin of one taxon could create new niche opportunities for other species to exploit, leading to the genesis of many new taxa in a process termed “sequential divergence.” Here, we test for such a multiplicative effect of sequential divergence in a community of host-specific parasitoid wasps,Diachasma alloeum, Utetes canaliculatus, andDiachasmimorpha mellea(Hymenoptera: Braconidae), that attackRhagoletis pomonellafruit flies (Diptera: Tephritidae). Flies in theR. pomonellaspecies complex radiated by sympatrically shifting and ecologically adapting to new host plants, the most recent example being the apple-infesting host race ofR. pomonellaformed via a host plant shift from hawthorn-infesting flies within the last 160 y. Using population genetics, field-based behavioral observations, host fruit odor discrimination assays, and analyses of life history timing, we show that the same host-related ecological selection pressures that differentially adapt and reproductively isolateRhagoletisto their respective host plants (host-associated differences in the timing of adult eclosion, host fruit odor preference and avoidance behaviors, and mating site fidelity) cascade through the ecosystem and induce host-associated genetic divergence for each of the three members of the parasitoid community. Thus, divergent selection at lower trophic levels can potentially multiplicatively and rapidly amplify biodiversity at higher levels on an ecological time scale, which may sequentially contribute to the rich diversity of life.