Rapid evolution of prey maintains predator diversity

Autoři: Akihiko Mougi aff001
Působiště autorů: Institute of Agricultural and Life Sciences, Academic Assembly, Shimane University, Nishikawatsu-cho, Matsue, Japan aff001
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227111


Factors maintaining the populations of diverse species that share limited resources or prey remain important issues in ecology. In the present study, I propose that heritable intraspecific variation in prey, which facilitates natural selection, is a key to solve this issue. A mathematical model reveals that diverse genotypes in a prey promote the coexistence of multiple predator species. When two predators share a prey with multiple genotypes, evolution nearly selects the two prey genotypes. Through analysis, I establish a condition of coexistence of such multiple predator–one prey interaction with two genotypes. If each prey type has high defensive capacity against different predator species, stable coexistence is likely to occur. Particularly, interspecific variations of life-history parameters allow the coexistence equilibrium to be stable. In addition, rapid evolution in a prey allows more than two predator species to coexist. Furthermore, mutation tends to stabilize otherwise unstable systems. These results suggest that intraspecific variation in a prey plays a key role in the maintenance of diverse predator species by driving adaptive evolution.

Klíčová slova:

Evolutionary adaptation – Population dynamics – Population genetics – Predation – Predator-prey dynamics – Species diversity – Species interactions – System stability


1. Gause GF, The struggle for existence. (New York, NY: Hafner Publishing Company, 1934).

2. Hutchinson GE, The paradox of the plankton. Am Nat 95, 137–145 (1961).

3. Volterra V, Variations and fluctuations of the number of individuals in animal species living together. J Cons Cons Int Explor Mer 3, 3–51 (1928).

4. MacArthur R, Levins R, Competition, habitat selection, and character displacement in a patchy environment. Proc Natl Acad Sci USA 51, 1207–1210 (1964). doi: 10.1073/pnas.51.6.1207 14215645

5. Rescigno A, Richardson IW, On the competitive exclusion principle. Bull Math Biophys 27, 85–89 (1965).

6. Levins R, Evolution in changing environments: some theoretical explorations. (Princeton Univ. Press, Princeton, NJ, 1968).

7. Levin SA, Community equilibria and stability, and an extension of the competitive exclusion principle. Am Nat 104, 413–423 (1970).

8. Hutchinson GE, Homage to santa rosalia or why are there so many kinds of animals? Am Nat 93, 145–159 (1959).

9. Chesson P, Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31, 343–366 (2000).

10. Levins R, Coexistence in variable environment. Am Nat 114, 765–783 (1979).

11. Chase JM, Abrams PA, Grover JP, Diehl S, Chesson P, Holt RD, et al. The interaction between predation and competition: a review and synthesis. Ecol Lett 5, 302–315 (2002).

12. Amarasekare P, Competitive coexistence in spatially structured environments: a synthesis. Ecol Lett 6, 1109–1122 (2003).

13. Huisman J, Weissing FJ, Biodiversity of plankton by species oscillations and chaos. Nature 402, 407–410 (1999).

14. Abrams PA, Holt RD, The impact of consumer-resource cycles on the coexistence of competing consumers. Theor Popul Biol 62, 281–295 (2002). doi: 10.1006/tpbi.2002.1614 12408947

15. Armstrong RA, Mcgehee R, Competitive-Exclusion. Am Nat 115, 151–170 (1980).

16. Haigh J, Maynard Smith J, Can there be more predators than prey? Theor Popul Biol 3, 290–299 (1972). doi: 10.1016/0040-5809(72)90005-6 4667088

17. Bolnick DI, Amarasekare P, Araújo MS, Bürger R, Levine JM, Novak M, et al. Why intraspecific trait variation matters in community ecology. Trend Ecol Evol 26, 183–192 (2011).

18. Schreiber SJ, Bürger R, Bolnick DI, The community effects of phenotypic and genetic variation within a predator population. Ecology 92, 1582–1593 (2011). doi: 10.1890/10-2071.1 21905425

19. Menden-Deuer S, Rowlett J, Many ways to stay in the game: individual variability maintains high biodiversity in planktonic microorganisms. J Royal Soc Inter 11, 20140031 (2014).

20. Menden-Deuer S, Rowlett J, The theory of games and microbe ecology. Theor Ecol 12, 1–15 (2019).

21. Schreiber SJ, Patel S, Terhorst C, Evolution as a coexistence mechanism: Does genetic architecture matter? Am Nat 191, 407–420 (2018).

22. Duffy MA, Ecological consequences of intraspecific variation in lake Daphnia. Freshw Biol 55, 995–1004 (2010).

23. Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, et al. The ecology of individuals: incidence and implications of individual specialization. Am Nat 161, 1–28 (2003). doi: 10.1086/343878 12650459

24. Lankau RA, Strauss SY, Mutual feedbacks maintain both genetic and species diversity in a plant community. Science 317, 1561–1563 (2007). doi: 10.1126/science.1147455 17872447

25. Roff DA, Evolutionary Quantitative Genetics (Chapman and Hall, 1997).

26. Lynch M, Walsh B, Genetics and Analysis of Quantitative Traits (Sinauer Associates, Inc, 1998).

27. Fussmann GF, Loreau M, Abrams PA, Eco-evolutionary dynamics of communities and ecosystems. Funct Ecol 21, 465–477 (2007).

28. Yoshida T, Jones LE, Ellner SP, Fussmann GF, Hairston NG Jr, Rapid evolution drives ecological dynamics in a predator-prey system. Nature 424, 303–306 (2003). doi: 10.1038/nature01767 12867979

29. Hairston NG Jr, Ellner SP, Geber M, Yoshida T, Fox JE, Rapid evolution and the convergence of ecological and evolutionary time. Ecol Lett 8, 1114–1127 (2005).

30. Bailey JK, Schweitzer JA, Úbeda F, Koricheva J, LeRoy CJ, Madritch MD, et al. From genes to ecosystems: a synthesis of the effects of plant genetic factors across levels of organization. Phil Trans Roy Soc B: Biol Sci 364, 1607–1616 (2009).

31. Jones LE, Becks L, Ellner SP, Hairston NG Jr, Yoshida T, Fussmann G, Rapid contemporary evolution and clonal food web dynamics. Phil Trans Roy Soc B: Biol Sci 364, 1579–1591 (2009).

32. Palkovacs EP, Marshall MC, Lamphere BA, Lynch BR, Weese DJ, Fraser DF, et al. Experimental evaluation of evolution and coevolution as agents of ecosystem change in Trinidadian streams. Phil Trans Roy Soc B: Biol Sci 364, 1617–1628 (2009).

33. Post DM, Palkovacs EP, Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play. Phil Trans Roy Soc B: Biol Sci 364, 1629–1640 (2009).

34. Abrams PA, The evolution of predator-prey interactions: theory and evidence. Annu Rev Ecol Syst 31, 79–105 (2000).

35. Cortez MH, Ellner SP, Understanding rapid evolution in predator-prey interactions using the theory of fast-slow dynamical systems. Am Nat 176, E109–E127 (2010). doi: 10.1086/656485 20863225

36. Mougi A, Iwasa Y, Evolution towards oscillation or stability in a predator-prey system. Proc R Soc B 277, 3163–3171 (2010). doi: 10.1098/rspb.2010.0691 20504808

37. Mougi Iwasa Y, Unique coevolutionary dynamics in a predator-prey system. J Theor Biol 277, 83–89 (2011). doi: 10.1016/j.jtbi.2011.02.015 21354181

38. Mougi A, Predator prey coevolution driven by size selective predation can cause anti-synchronized and cryptic population dynamics. Theor Popul Biol 81,113–118 (2012). doi: 10.1016/j.tpb.2011.12.005 22212374

39. Cortez MH, Weitz JS, Coevolution can reverse predator-prey cycles. Proc Nat Acad Sci USA 111, 7486–7491 (2014). doi: 10.1073/pnas.1317693111 24799689

40. Klauschies T, Vasseur DA, Gaedke U, Trait adaptation promotes species coexistence in diverse predator and prey communities. Ecol Evol 6, 4141–4159 (2016). doi: 10.1002/ece3.2172 27516870

41. Klauschies T, Coutinho RM, Gaedke U, A beta distribution-based moment closure enhances the reliability of trait-based aggregate models for natural populations and communities. Ecol Model 381, 46–77 (2018).

42. Taylor PD, Jonker LB, Evolutionary stable strategies and game dynamics. Math Biosci 40,145–156 (1978).

43. Schuster P, Sigmund K, Replicator dynamics. J Theor Biol 100, 533–538 (1983).

44. Tilman D, Resources: a graphical-mechanistic approach to competition and predation. Am Nat 116, 363–393 (1980).

45. Abrams PA, The prerequisites for and likelihood of generalist-specialist coexistence. Am Nat 167, 329–342 (2006). doi: 10.1086/499382 16673342

46. Gillespie JH, Pleiotropic overdominance and the maintenance of genetic variation in polygenic characters. Genetics 107, 321–330 (1984). 6735172

47. Gillespie JH, Turelli M, Genotype-environment interactions and the maintenance of polygenic variation. Genetics 121, 129–138 (1989). 17246488

48. Frankhan R, Genetics and extinction. Biol Conserv 126, 131–140 (2005).

Článek vyšel v časopise


2019 Číslo 12
Nejčtenější tento týden