Sequential divergence and the multiplicative origin of community diversity Glen R. Hooda,1, Andrew A. Forbesb, Thomas H. Q. Powella,c, Scott P. Egana,d,e, Gabriela Hamerlinckb, James J. Smithf, and Jeffrey L. Federa,d aDepartment of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556; bDepartment of Biology, University of Iowa, Iowa City, IA 52242; cDepartment of Entomology and Nematology, University of Florida, Gainesville, FL 32611; dEnvironmental Change Initiative and Advanced Diagnostics and Therapeutics, University of Notre Dame, Notre Dame, IN 46556; eDepartment of Biosciences, Anderson Biological Laboratories, Rice University, Houston, TX 77005; and fDepartment of Entomology and Lyman Briggs College, Michigan State University, East Lansing, MI 48824 Edited by Douglas Futuyma, State University of New York, Stony Brook, NY, and approved September 18, 2015 (received for review December 24, 2014) Phenotypic and genetic variation in one species can influence the Such “sequential” or “cascading” divergence events may be composition of interacting organisms within communities and across particularly relevant to understanding why some groups of or- ecosystems. As a result, the divergence of one species may not be an ganisms, like plants, the insects that feed on them, and the para- isolated process, as the origin of one taxon could create new niche sitoids that attack the insects, are more diverse and species-rich than – opportunities for other species to exploit, leading to the genesis of other groups (8, 9, 12 15). Specifically, when phytophagous insects many new taxa in a process termed “sequential divergence.” Here, diversify by adapting to new host plants, they create a new habitat we test for such a multiplicative effect of sequential divergence in a for their parasitoids to exploit (Fig. 1). If a parasitoid shifts to the community of host-specific parasitoid wasps, Diachasma alloeum, new habitat, it can encounter the same divergent ecological selec- tion pressures as its insect host, which could result in the parallel Utetes canaliculatus,andDiachasmimorpha mellea (Hymenoptera: divergence of insect host and parasitoid (12–15) (Fig. 1A). More- Braconidae), that attack Rhagoletis pomonella fruit flies (Diptera: over, sequential divergence may have multiplicative effects in gen- Tephritidae). Flies in the R. pomonella species complex radiated by erating biodiversity, as the shift of an insect to a new plant may open sympatrically shifting and ecologically adapting to new host plants, a new niche opportunity for not just one but the entire community the most recent example being the apple-infesting host race of of parasitoids attacking the insect host (12, 13) (Fig. 1B). However, R. pomonella formed via a host plant shift from hawthorn-infesting few convincing examples of sequential divergence exist (12–15), and flies within the last 160 y. Using population genetics, field-based in no study is there both genetic and ecological evidence for behavioral observations, host fruit odor discrimination assays, and sequential divergence multiplicatively amplifying biodiversity. analyses of life history timing, we show that the same host-related Here, we test for the multiplicative effects of sequential di- ecological selection pressures that differentially adapt and reproduc- vergence in the community of parasitoid wasps (Hymenoptera: tively isolate Rhagoletis to their respective host plants (host-associated Braconidae) that attack fruit flies in the Rhagoletis pomonella differences in the timing of adult eclosion, host fruit odor preference sibling species complex (Diptera: Tephritidae) (Fig. 2). Several and avoidance behaviors, and mating site fidelity) cascade through the features of the biology and biogeography of the Rhagoletis−para- ecosystem and induce host-associated genetic divergence for each of sitoid system make it ideal for investigating the multiplicative the three members of the parasitoid community. Thus, divergent se- divergence hypothesis and allow us to directly test multiple criteria lection at lower trophic levels can potentially multiplicatively and rap- supporting sympatric host race formation (16) and sequential di- idly amplify biodiversity at higher levels on an ecological time scale, vergence (12, 13), summarized in Table 1. First, concerning the which may sequentially contribute to the rich diversity of life. spatial context of divergence (criterion 1), R. pomonella complex host plant adaptation | parasitoid | Rhagoletis | tritrophic interactions | Significance ecological speciation Understanding how new life forms originate is a central question opulation divergence is a fundamental evolutionary process in biology. Population divergence is usually studied with respect Pcontributing to the diversity of life (1). Studies of how new life to how single lineages diverge into daughter taxa. However, forms originate typically focus on how barriers to gene flow evolve populations may not always differentiate in isolation; divergence in specific lineages, resulting in their divergence into descendent of one taxon could create new niche opportunities in higher tro- daughter taxa. As a result, evolutionary biologists now have a good phic levels, leading to the sequential origin of many new taxa. Here, we show that this may be occurring for three species of understanding of how variation within a population is trans- parasitoid wasps attacking Rhagoletis fruit flies. As flies shift and formed by selection into differences between taxa (1–3). What is adapt to new host plants, wasps follow suit and diverge in kind, less well understood is whether the divergence of one population resulting in a multiplicative increase of diversity as the effects of has consequences that ripple through the trophic levels of an ecologically based divergent selection cascade through the eco- ecosystem and affect entire communities of interacting organ- system. Biodiversity therefore may potentially beget increasing – isms. Studies in paleontology (4 6), community ecology (7, 8), levels of biodiversity. systematics (8, 9), and ecosystem genetics (10, 11) suggest that evolutionary change in one lineage can influence entire com- Author contributions: G.R.H., A.A.F., T.H.Q.P., S.P.E., and J.L.F. designed research; G.R.H., munities of organisms. For example, when the genotype/pheno- A.A.F., T.H.Q.P., S.P.E., G.H., J.J.S., and J.L.F. performed research; G.R.H., A.A.F., T.H.Q.P., and type of a “foundation” species influences the relative fitness of J.L.F. contributed new reagents/analytic tools; G.R.H., A.A.F., S.P.E., G.H., and J.L.F. analyzed data; and G.R.H., A.A.F., T.H.Q.P., S.P.E., G.H., J.J.S., and J.L.F. wrote the paper. other species, evolutionary change(s) in this genotype/phenotype The authors declare no conflict of interest. may affect organisms in adjacent trophic levels (10, 11). If these evolutionary changes are linked to ecological adaptation and re- This article is a PNAS Direct Submission. Data deposition: The mtDNA sequences reported in this paper have been deposited in the productive isolation (RI), associated organisms may diverge in par- GenBank database (accession nos. KT761291–KT761497). Raw data are available from the allel, potentially creating entire coevolved communities distinct from Dryad Digital Repository, dx.doi.org/10.5061/dryad.5n72m. – one another (12 15). Therefore, population divergence may not 1To whom correspondence should be addressed. Email: [email protected]. always be an isolated process, as the differentiation of one taxon This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. could beget the divergence of many others. 1073/pnas.1424717112/-/DCSupplemental. E5980–E5989 | PNAS | Published online October 23, 2015 www.pnas.org/cgi/doi/10.1073/pnas.1424717112 Downloaded by guest on October 1, 2021 Multiplicative Co-speciation PNAS PLUS Sequential Divergence Sequential Divergence in Allopatry A B C Fig. 1. Three scenarios of codivergence in a host− parasitoid system. (A) A single sequential divergence event, (B) sequential divergence with multiplicative amplification of biodiversity, and (C) cospeciation in allopatry. In A, codivergence is driven by the cas- Allopatry cade of divergent ecological selection pressures across trophic levels in sympatry. Here, a degree of divergent ecological adaptation must accompany the host shift such that parasitoids are not merely moving between geographically separated hosts. In Time Time B, the multiplicative effects of sequential divergence can be seen as several members of the parasitoid community diverge in parallel with their host. In C, Secondary contact codivergence (cospeciation) occurs after host plant, fly, and parasitoid populations become jointly geo- graphically isolated (black bar), resulting in parallel allopatric speciation. Here, little differentiation need accompany the initial host shift of fly or parasitoid. Cospeciation is not necessarily driven by the creation and adaptation to new niches but by the concordant geographic and reproductive separation of hosts and parasitoids. flies have formed in the absence of geographic isolation. In par- vergence (14). Population genetic surveys, field observations, EVOLUTION ticular, the recent sympatric shift of R. pomonella from its ancestral behavioral assays of host choice, and studies of life history timing host plant hawthorn (Crataegus spp.) to introduced domesticated support the existence of an ecologically derived population of apple (Malus domestica)