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Effects of Rapid Evolution on Species Coexistence

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Effects of Rapid Evolution on Species Coexistence Effects of rapid evolution on species coexistence Simon P. Harta,1,2, Martin M. Turcotteb,1, and Jonathan M. Levinea,3 aInstitute of Integrative Biology, ETH Zürich, 8092 Zürich, Switzerland; and bDepartment of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260 Edited by Dolph Schluter, University of British Columbia, Vancouver, BC, Canada, and approved November 30, 2018 (received for review October 3, 2018) Increasing evidence for rapid evolution suggests that the mainte- more likely when opportunities for the evolution of niche differentia- nance of species diversity in ecological communities may be tion are limited, as occurs when species cannot substitute other influenced by more than purely ecological processes. Classic theory resources for the ones used by their competitors (24, 25). In general shows that interspecific competition may select for traits that then, it remains unclear how competitive population dynamics increase niche differentiation, weakening competition and thus should change as a consequence of evolution, and the resulting eco- promoting species coexistence. While empirical work has demon- evolutionary feedbacks could be more complex than is generally strated trait evolution in response to competition, if and how appreciated (16, 20). evolution affects the dynamics of the competing species—the key A third reason for poorly resolved empirical evidence for com- step for completing the required eco-evolutionary feedback—has been petitive, eco-evolutionary feedbacks relates to the concurrent nature difficult to resolve. Here, we show that evolution in response to inter- of the ecological and evolutionary changes. If ecological and evo- lutionary processes simultaneously feed back on one another, this specific competition feeds back to change the course of competitive – dynamic cannot be resolved by assuming a separation of timescales, population dynamics of aquatic plant species over 10 15 generations and quantifying the population-dynamic consequences of past evo- in the field. By manipulating selection imposed by heterospecific com- i lutionary change (15, 26). These three limitations have motivated petitors in experimental ponds, we demonstrate that ( ) interspecific recent calls for combining experimental evolution approaches (8) ii competition drives rapid genotypic change, and ( ) this evolutionary more typical of studies in laboratory microbial systems (27) with the change in one competitor, while not changing the coexistence outcome, tools of quantitative coexistence theory (16) to understand how rapid causes the population trajectories of the two competing species to con- evolution in response to competition affects species coexistence in verge. In contrast to the common expectation that interspecific compe- more natural systems. tition should drive the evolution of niche differentiation, our results Here, we demonstrate how eco-evolutionary feedbacks influ- ECOLOGY suggest that genotypic evolution resulted in phenotypic changes that ence coexistence by experimentally manipulating the ability altered population dynamics by affecting the competitive hierarchy. This of aquatic plant species to evolve in response to interspecific result is consistent with theory suggesting that competition for essential competition while simultaneously quantifying their multigener- resources can limit opportunities for the evolution of niche differentia- ational competitive population dynamics. Our approach allows tion. Our finding that rapid evolution regulates the dynamics of com- us to address three questions: (i) Does interspecific competition peting species suggests that ecosystems may rely on continuous cause evolutionary change on ecological timescales? (ii) Is this feedbacks between ecology and evolution to maintain species diversity. evolutionary change consistent and large enough to alter the contemporary dynamics of the competing species? And, (iii) how biodiversity | eco-evolutionary dynamics | competition | character displacement | diversity maintenance Significance lassic theory suggests that natural selection arising from in- Understanding the dynamics of competing species is essential Cterspecific competition should generate phenotypic differences for explaining the origin and maintenance of species diversity. between species that weaken interspecific competition, favoring However, ecologists have typically ignored the potential for species coexistence (1–5). However, while this eco-evolutionary rapid evolution to alter the contemporary population dynamics process has become central to explanations for diversity (6, 7), em- of competing species. By disrupting the ability of aquatic plants pirical evidence for such feedbacks between ecology and evolution to evolve in response to interspecific competition, we show that remain equivocal for three reasons (8). First, evolution in response to competition drives evolutionary change and this evolutionary interspecific competition is most commonly inferred from post hoc change simultaneously feeds back to alter the abundance of observational evidence that morphological differences between spe- competing species over just a few generations. Rather than in- ciesarelargerwhenspeciesoccurtogether(insympatry)vs.apart(in creasing niche differences as classic theory predicts, evolution allopatry) (8–10), with the strongest evidence coming from natural causes population trajectories to converge by changing the com- experiments (11, 12). While a few experimental studies demonstrate petitive hierarchy. Our results suggest that understanding how trait change in response to interspecific competition (13, 14), the species diversity is maintained requires explicitly accounting for the causal influence of competition, the repeatability of the evolutionary effects of rapid evolution on competitive population dynamics. change, and the speed of evolution relative to the rate of competitive population dynamics are often unknown (8). Author contributions: S.P.H., M.M.T., and J.M.L. designed research; S.P.H. and M.M.T. per- formed experiments; M.M.T. led the laboratory genetic analyses; S.P.H. analyzed data; and Second, and maybe more importantly, while the feedback from S.P.H. wrote the first draft of the paper and all authors contributed substantially to revisions. evolutionary change to the population dynamics of the competing The authors declare no conflict of interest. species is essential for contemporary evolution to affect diversity maintenance, this feedback is rarely empirically quantified (8, 15, 16). This article is a PNAS Direct Submission. In lieu of direct empirical evidence, population dynamic conse- Published under the PNAS license. quences are typically assumed following the common theoretical Data Deposition: Data relating to this work have been deposited on figshare (doi: 10. expectation that evolved trait and behavioral differences should 6084/m9.figshare.7599095.v1). promote coexistence by increasing niche differences (7, 8, 11, 17–19). 1S.P.H. and M.M.T. contributed equally to this work. However, as emphasized in recent reviews, the assumption that 3Present address: Department of Ecology and Evolutionary Biology, Princeton University, evolution should increase niche differences may not always be justi- Princeton, NJ 08544. fied (16, 20). Developments in species coexistence theory demon- 2To whom correspondence should be addressed. Email: [email protected]. strate an equally important role for differences between species in This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. competitive ability in determining competitive outcomes (21–23). 1073/pnas.1816298116/-/DCSupplemental. Indeed, theory suggests that evolution of competitive ability may be www.pnas.org/cgi/doi/10.1073/pnas.1816298116 PNAS Latest Articles | 1of6 Downloaded by guest on September 30, 2021 does this feedback influence coexistence via the evolution of A niche differences and/or species’ competitive abilities? To an- 0.3 swer these questions, we studied two species of floating, aquatic conspecific heterospecific plants—Lemna minor and Spirodela polyrhiza. Both species have fast life cycles with asexual reproduction every 3–7dand∼20 gen- selection selection erations per growing season (28), providing an ideal system for understanding how eco-evolutionary feedbacks affect the con- temporary dynamics of competing species. 0.1 0.2 We imposed two selection treatments on multigenotype pop- ulations of the two species competing in replicate experimental ponds in the field (Materials and Methods). In the “heterospecific selection” treatment, the two species competed with each other in genotype frequency competitivearenasandwerefreetoevolveinresponsetoin- terspecific competition. In the “conspecific selection” treatment, the −0.1 0.0 123456789123456789 two species also competed with each other, but in this treatment we L. minor genotypes prevented evolution in response to interspecific competition. We did B so by replacing all individuals in these competitive arenas every 2 wk with the same number of individuals of each species, but drawn from conspecific heterospecific multigenotype populations growing and evolving in single-species selection selection monocultures in the same ponds. Thus, our experimental manipu- lation preserves the ongoing effects of interspecific competition on the population sizes of the two species, but prevents evolution in response to interspecific competition, and thereby prevents this evolution from affecting
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