vol. 195, no. 4 the american naturalist april 2020 E-Comment Competitive Exclusion and Evolution: Convergence Almost Never Produces Ecologically Equivalent Species (A Comment on McPeek, “Limiting Similarity? The Ecological Dynamics of Natural Selection among Resources and Consumers Caused by Both Apparent and Resource Competition”) Liz Pásztor,1,* György Barabás,2,3 and Géza Meszéna3,4 1. Department of Genetics, Eötvös Loránd University (ELTE), Budapest, Hungary; and Hungarian Academy of Sciences (MTA) Centre for Ecological Research, Tihany H-8237 Klebelsberg Kuno u. 3, Budapest, Hungary; 2. Division of Theoretical Biology, Department of Physics, Chemistry, and Biology (IFM), Linköping University, Linköping, Sweden; 3. MTA-ELTE Theoretical Biology and Evolutionary Ecology Research Group, ELTE, Budapest, Hungary; 4. Department of Biological Physics, ELTE, Budapest, Hungary Submitted July 22, 2019; Accepted November 11, 2019; Electronically published February 28, 2020 abstract: In a recent modeling study (“Limiting Similarity? The investigates the possibility of the emergence of neutral co- Ecological Dynamics of Natural Selection among Resources and existence via convergent evolution besides discussing op- Consumers Caused by Both Apparent and Resource Competition”) portunities for divergence. McPeek emphasizes that his that appeared in the April 2019 issue of The American Naturalist, results contrast with expectations from naive versions of Mark A. McPeek argued that ecologically equivalent species may the limiting similarity principle and argues for supple- emerge via competition-induced trait convergence, in conflict with menting the purely ecological study of conditions for co- naive expectations based on the limiting similarity principle. Al- existence with the explicit modeling of evolutionary dy- though the emphasis on the possibility of the convergence of compet- itors is very timely, here we show that the proposed mechanism will namics. This is an important point, and McPeek (2019) only lead to actual coexistence in the converged state for specially makes a great contribution by emphasizing it in a remark- chosen fine-tuned parameter settings. It is therefore not a robust mech- ably clear way. However, we feel compelled to clarify how anism for the evolution of ecologically equivalent species. We conclude the principle of limiting similarity in fact still applies to that invoking trait convergence as an explanation for the co-occurrence McPeek’s conclusions, not only because a series of our of seemingly fully equivalent species in nature would be premature. own work was cited as supporting the naive expectations Keywords: neutral species, competition, adaptive dynamics, cryptic but also because of the central role played by this princi- species, character displacement, coexistence theory. ple in coexistence theory. We agree with McPeek that the co-occurrence of identical species differing only in neu- tral traits is a theoretical possibility. However, we wish Niche segregation and neutrality—or perhaps the contin- to show that competition-driven convergence to neutral- uum between these two extremes—have been considered ity will happen only under highly restrictive conditions. as possible explanations of species co-occurrence (Holt It is therefore unlikely to be an explanation for the long- 2006; Adler et al. 2007; Rapacciuolo and Blois 2019). term co-occurrence of competing cryptic or sister species. While there are strong theoretical arguments (Chesson Hence, we wish to clarify the relationship between robust- 1991) and ample empirical evidence (Janzen et al. 2017) ness of coexistence and similarity, to specify the relevance for niche segregation, there are also several observations of the principle of weak limiting similarity (Meszéna et al. of the co-occurrence of reproductively isolated species with 2006; Burgess et al. 2019) for McPeek’s (2019) model via no obvious ecological differentiation between them (McPeek simulations of evolutionary trajectories, and to discuss the and Gomulkiewicz 2005). In a recent article, McPeek (2019) problem of convergence within the universal framework of adaptive dynamics. At the end we summarize the con- * Corresponding author; email: [email protected]. clusions for the emergence of species. ORCIDs: Pásztor, https://orcid.org/0000-0003-2630-5673; Barabás, https:// orcid.org/0000-0002-7355-3664; Meszéna, https://orcid.org/0000-0002-6557 -8423. Robustness and the Weak Limiting Similarity Principle Am. Nat. 2020. Vol. 195, pp. E112–E117. q 2020 by The University of Chicago. 0003-0147/2020/19504-59381$15.00. All rights reserved. Competition-driven convergence seems to contradict the DOI: 10.1086/707610 principle of limiting similarity. If such convergence leads This content downloaded from 130.236.088.106 on August 10, 2020 01:34:06 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). (E-comment) Competitive Exclusion and Evolution E113 to completely identical species whose relative densities to discern. In fact, it is easier than it seems at first sight. fluctuate via ecological drift, their long-term coexistence Evolving away from consuming an already heavily ex- is expected as long as their population sizes are sufficiently ploited resource is advantageous only if a different re- large (McPeek and Gomulkiewicz 2005). Such neutrality is source is available and the diet change does not incur large robust in the face of environmental disturbances, as the en- fitness costs. Assume that two species with widely different vironmental response functions of two biologically identi- diets arrive in a habitat with narrow resource diversity. cal species are also identical. Thus, two completely identi- They will evolve convergently, as both species will adapt cal species may coexist, and their coexistence is robust to to the resource distribution existing in the new habitat. environmental disturbances. Robustness of a system’s be- Convergent evolution either leads to their coexistence with havior to parametric uncertainties is an important concept, smaller diet differentiation or to one of them being lost via not only for niche theory (Chesson 1991) but also for sys- the strengthening competition (Germain et al. 2018). tems biology—for example, in the context of morphogen- McPeek’s model considers two resource and two con- esis (Eldar et al. 2004), in metabolic and gene regulatory sumer populations, each characterized by the phenotypic networks (Nijhout et al. 2019), and in engineering (Aström distribution (mean and variance) of a quantitative trait. In- and Murray 2008). In general, robustness is a consequence teractions between the species induce frequency-dependent of differences between negative feedback loops. Too much selection on the means of these distributions. The instanta- similarity in feedback structure results in diminished ro- neous per capita population growth rates define the popu- bustness. The weak limiting similarity principle claims that lation fitness values, which are in turn composed of the the coexistence of a given set of (nonidentical) populations contributions from all phenotypes within those popula- is restricted to a narrow range of the externally determined tions. Trait evolution is governed by quantitative genetic parameters when the overlap is large between either the rules (Taper and Case 1985) while the ecological dynamics “impact” niche or the “sensitivity” niche of the populations bears most resemblance to MacArthur’s(1972)modelof (Meszéna et al. 2006; called the “principle of robust coex- resource competition, due to a self-regulation term that ef- istence” in Pásztor et al. 2016). In the context of Mac- fectively makes resource growth logistic in the absence of Arthur and Levins (1967), coexistence is sufficiently robust consumption (this also means that resource supply is not when the competing species are roughly separated by the modeled as in Tilman 1982, with biotic resources assumed niche width defined by the resource utilization function— instead). The model is similar in spirit to quantitative ge- otherwise, coexistence becomes very sensitive to parameter netic models of competition along a trait axis, where the perturbations (Szabó and Meszéna 2006). As a consequence, more similar the consumers are in their trait, the more sim- while two identical species may coexist, any difference be- ilarly they consume the resources and so the more they tween their functional traits makes their coexistence prone compete (Slatkin 1980; Taper and Case 1985; Schreiber to changes in the external environment. Moreover, random et al. 2011; Vasseur et al. 2011; Barabás and D’Andrea genetic mutations turn the coexistence of two identical spe- 2016). The difference is that in the model of McPeek, the cies structurally unstable in the long run: a mutation pro- resource populations themselves may evolve to provide a viding a slight difference in fitness will lead to competitive better or worse match with the traits of their consumers. exclusion. Focusing here on the case of convergence, figure 1A As McPeek (2019) correctly emphasizes, the validity of reproduces one such scenario, taken straight from McPeek the weak limiting similarity principle does not guarantee (2019). The dynamics end up with the co-occurrence of divergent evolution. This purely ecological principle as- two ecologically identical species. As mentioned before, sumes fixed species. Still, it does apply at each step of any however, such coexistence