What Are the Fundamental Questions Regarding Evolution in Ecological Networks?
Authors: Axel G. Rossberg
Journal: Trends in Ecology & Evolution (2020)

Reviewing ‘The Role of Evolution in Shaping Ecological Networks’ by Segar et al. [1.Segar S.T. et al.The role of evolution in shaping ecological networks.Trends Ecol. Evol. 2020; 35: 454-466Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar] stirred controversy over the central question [2.Sagoff M. Ecological networks: response to Segar et al..Trends Ecol. Evol. 2020; 35: 862-863Abstract Full Text Full Text PDF PubMed Scopus (2) Google Scholar]. I propose to settle this by defining concepts more clearly, answer other outstanding questions raised by Segar et al., and draw attention to some very different related open fundamental questions. Adjacency matrices of ecological networks are thresholded matrices of interaction strengths [3.Rossberg A.G. et al.Universal power-law diet partitioning by marine fish and squid with surprising stability-diversity implications.Proc. Biol. Sci. 2011; 278: 1617-1625Crossref PubMed Scopus (15) Google Scholar,4.Rossberg A.G. Food Webs and Biodiversity: Foundations, Models, Data. Wiley, 2013Crossref Scopus (61) Google Scholar. Denote for any two species, i, j by Aij the strength of the directed interaction (of a particular type) between them, defined such that these values are robust to variation in the abundance of i, j and other species–for trophic interactions as the attack-rate parameter in a fitted functional response [5.Berlow E.L. et al.Interaction strengths in food webs: issues and opportunities.J. Anim. Ecol. 2004; 73: 585-598Crossref Scopus (417) Google Scholar]. The idea that ‘patterns in networks are mediated by species-specific traits’ [1.Segar S.T. et al.The role of evolution in shaping ecological networks.Trends Ecol. Evol. 2020; 35: 454-466Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar] has been formalised [4.Rossberg A.G. Food Webs and Biodiversity: Foundations, Models, Data. Wiley, 2013Crossref Scopus (61) Google Scholar] by the condition that there is a function ã such thatAij=ã(ti,tj),[1] where, for any species k, the vector tk provides quantitative characterisations of all its ecologically relevant traits. The idea of traits specific to particular ecological roles (e.g., ‘consumer traits’ [1.Segar S.T. et al.The role of evolution in shaping ecological networks.Trends Ecol. Evol. 2020; 35: 454-466Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar]), has been formalised [4.Rossberg A.G. Food Webs and Biodiversity: Foundations, Models, Data. Wiley, 2013Crossref Scopus (61) Google Scholar] by the condition that there are continuous functions V and F mapping trait vectors t into lower-dimensional trait spaces such that, for some continuous function a, Aij≈aV(ti),F(tj).[2] Defining for any species k its 'vulnerability traits' as vk = V (tk) and its 'foraging traits' as fk = F (tk), Aij≈avi,fj.[3] Network evolution must be modelled through the evolution of these traits–which answers the second ‘Outstanding Question’ of [1.Segar S.T. et al.The role of evolution in shaping ecological networks.Trends Ecol. Evol. 2020; 35: 454-466Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar]. Modelling the Aij directly as ‘evolving traits’ [1.Segar S.T. et al.The role of evolution in shaping ecological networks.Trends Ecol. Evol. 2020; 35: 454-466Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar] leads to artefacts [6.Rossberg A.G. et al.Food webs: experts consuming families of experts.J. Theor. Biol. 2006; 241: 552-563Crossref PubMed Scopus (94) Google Scholar]. The idea of trait ‘matching’ [1.Segar S.T. et al.The role of evolution in shaping ecological networks.Trends Ecol. Evol. 2020; 35: 454-466Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar,6.Rossberg A.G. et al.Food webs: experts consuming families of experts.J. Theor. Biol. 2006; 241: 552-563Crossref PubMed Scopus (94) Google Scholar between interaction partners such as consumers and resources is captured by generic models for the function a such as [4.Rossberg A.G. Food Webs and Biodiversity: Foundations, Models, Data. Wiley, 2013Crossref Scopus (61) Google Scholar]a(v,f)=a0expv0+f0−12∑k=1Dσk(vk−fk)2,[4] with D denoting the dimensionality of trophic niche space and v0,…,vD and f0,…,fD the components of v and f, respectively. The constant a0 has the appropriate dimensions and σk = ±1 [4.Rossberg A.G. Food Webs and Biodiversity: Foundations, Models, Data. Wiley, 2013Crossref Scopus (61) Google Scholar]. When imposing a condition that the sum of v02 over all species is minimised, f- and v-vectors are uniquely determined up to rigid geometric transformations, thus, crucial for the following, reproducibly characterising species rather than data sets [4.Rossberg A.G. Food Webs and Biodiversity: Foundations, Models, Data. Wiley, 2013Crossref Scopus (61) Google Scholar]. In this setting, a perfect ‘match’ means equality of all but the first components of v and f [4.Rossberg A.G. Food Webs and Biodiversity: Foundations, Models, Data. Wiley, 2013Crossref Scopus (61) Google Scholar]. Equation 4 can be expressed in the equivalent form [6.Rossberg A.G. et al.Food webs: experts consuming families of experts.J. Theor. Biol. 2006; 241: 552-563Crossref PubMed Scopus (94) Google Scholar,7.Rohr R.P. et al.Modeling food webs: exploring unexplained structure using latent traits.Am. Nat. 2010; 176: 170-177Crossref PubMed Scopus (73) Google Scholar a(v,f)=a^(v^0,v^,f^0,f^)=a0expv^0+f^0+v^⋅f^,[5] with the number v^0 and the D-component vector v^ given by v, and f^0, f^ given by f [4.Rossberg A.G. Food Webs and Biodiversity: Foundations, Models, Data. Wiley, 2013Crossref Scopus (61) Google Scholar]. Both formulations, Equations 4 and 5, have been empirically verified for food webs [4.Rossberg A.G. Food Webs and Biodiversity: Foundations, Models, Data. Wiley, 2013Crossref Scopus (61) Google Scholar,7.Rohr R.P. et al.Modeling food webs: exploring unexplained structure using latent traits.Am. Nat. 2010; 176: 170-177Crossref PubMed Scopus (73) Google Scholar, but are applicable more widely. Segar et al. [1.Segar S.T. et al.The role of evolution in shaping ecological networks.Trends Ecol. Evol. 2020; 35: 454-466Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar] and Sagoff [2.Sagoff M. Ecological networks: response to Segar et al..Trends Ecol. Evol. 2020; 35: 862-863Abstract Full Text Full Text PDF PubMed Scopus (2) Google Scholar] differ over whether ‘The structure of ecological networks reflects the evolutionary history of their biotic components’. As a general statement, this is correct in two different but weak senses. First, because, at the fundamental level, ecological interactions, ecology, and evolution are inseparable [10.Govaert L. et al.Eco-evolutionary feedbacks —theoretical models and perspectives.Funct. Ecol. 2019; 33: 13-30Crossref Scopus (71) Google Scholar]. Second, in terms of phylogenetic signal. By Equation (3), phylogenetic signal arises in networks if there is phylogenetic signal in the v-traits or the f-traits, but not necessarily in both, as Segar et al. appear to suggest. In food webs, for example, v-traits evolve much slower than f-traits, leading to stronger phylogenetic signal [6.Rossberg A.G. et al.Food webs: experts consuming families of experts.J. Theor. Biol. 2006; 241: 552-563Crossref PubMed Scopus (94) Google Scholar,8.Bersier L.F. Kehrli P. The signature of phylogenetic constraints on food-web structure.Ecol. Complex. 2008; 5: 132-139Crossref Scopus (75) Google Scholar (Figure 1). This, combined with a large-eats-small rule, is sufficient to produce food webs with highly realistic network properties [6.Rossberg A.G. et al.Food webs: experts consuming families of experts.J. Theor. Biol. 2006; 241: 552-563Crossref PubMed Scopus (94) Google Scholar,4.Rossberg A.G. Food Webs and Biodiversity: Foundations, Models, Data. Wiley, 2013Crossref Scopus (61) Google Scholar (answering the fifth ‘Outstanding Question’ of [1.Segar S.T. et al.The role of evolution in shaping ecological networks.Trends Ecol. Evol. 2020; 35: 454-466Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar]). Thus, network structure reflects evolutionary history: some birds feed on insects, others on weeds, yet most birds could fall prey to peregrine falcons. This is common knowledge. More interesting, though, is the question under which conditions evolutionary change in the v-traits of taxa gets into lockstep with f-traits of closely matching taxa. Plausibly, this requires frequent co-occurrence of the two taxa. Because, as Sagoff [2.Sagoff M. Ecological networks: response to Segar et al..Trends Ecol. Evol. 2020; 35: 862-863Abstract Full Text Full Text PDF PubMed Scopus (2) Google Scholar] explains, such close associations are, for species, the exception rather than the rule, so should be these coevolution or tracking phenomena. Instead, community turnover through space and time generates ever-changing fitness seascapes [11.Mustonen V. Lässig M. From fitness landscapes to seascapes: non-equilibrium dynamics of selection and adaptation..Trends Genet. 2009; 25: 111-119Abstract Full Text Full Text PDF PubMed Scopus (144) Google Scholar], driving random-walk evolution of v- and f-traits. Correspondingly, pairwise link-strength distributions are consistent with random expectation [3.Rossberg A.G. et al.Universal power-law diet partitioning by marine fish and squid with surprising stability-diversity implications.Proc. Biol. Sci. 2011; 278: 1617-1625Crossref PubMed Scopus (15) Google Scholar]. Transitions between tracking and losing track of close interaction partners are empirically well described [12.Clayton D.H. et al.Coevolution of Life on Hosts: Integrating Ecology and History. University of Chicago Press, 2015Crossref Google Scholar]. However, reliance on network modularity (block structure in adjacency matrices) as evidence for cases of tracking or coevolution phenomena [1.Segar S.T. et al.The role of evolution in shaping ecological networks.Trends Ecol. Evol. 2020; 35: 454-466Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar] risks overestimating their prevalence. Uncorrelated phylogenetic signals in v- and f-traits already generate such patterns [4.Rossberg A.G. Food Webs and Biodiversity: Foundations, Models, Data. Wiley, 2013Crossref Scopus (61) Google Scholar,6.Rossberg A.G. et al.Food webs: experts consuming families of experts.J. Theor. Biol. 2006; 241: 552-563Crossref PubMed Scopus (94) Google Scholar (Figure 1). A fundamental question arising from these considerations is why, despite phylogeny being so deeply imprinted in network structure, it appears of little relevance for explaining high-level ecological phenomena. The Population Dynamical Matching Model, for example, which combines phylogenetically structured assembly with coevolutionary feedbacks through direct and indirect trophic interactions, is highly successful in reproducing not only network structure [13.Rossberg A.G. et al.The top-down mechanism for body-mass-abundance scaling.Ecology. 2008; 89: 567-580Crossref PubMed Scopus (68) Google Scholar], but also macroecological characteristics [4.Rossberg A.G. Food Webs and Biodiversity: Foundations, Models, Data. Wiley, 2013Crossref Scopus (61) Google Scholar,13.Rossberg A.G. et al.The top-down mechanism for body-mass-abundance scaling.Ecology. 2008; 89: 567-580Crossref PubMed Scopus (68) Google Scholar,14.Fung T. et al.Impact of biodiversity loss on production in complex marine food webs mitigated by prey-release.Nat. Commun. 2015; 6: 6657Crossref PubMed Scopus (27) Google Scholar of observed communities (thus answering the first ‘Outstanding Question’ of [1.Segar S.T. et al.The role of evolution in shaping ecological networks.Trends Ecol. Evol. 2020; 35: 454-466Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar]). Yet, the mathematical explanations of these characteristics [4.Rossberg A.G. Food Webs and Biodiversity: Foundations, Models, Data. Wiley, 2013Crossref Scopus (61) Google Scholar] scarcely draw on the phylogenetic structure. This is not to say that evolution can ultimately be disregarded. For example, there is evidence for network-level selection of key parameters, such as baseline foraging traits f0 [4.Rossberg A.G. Food Webs and Biodiversity: Foundations, Models, Data. Wiley, 2013Crossref Scopus (61) Google Scholar,13.Rossberg A.G. et al.The top-down mechanism for body-mass-abundance scaling.Ecology. 2008; 89: 567-580Crossref PubMed Scopus (68) Google Scholar, dietary diversity [3.Rossberg A.G. et al.Universal power-law diet partitioning by marine fish and squid with surprising stability-diversity implications.Proc. Biol. Sci. 2011; 278: 1617-1625Crossref PubMed Scopus (15) Google Scholar,4.Rossberg A.G. Food Webs and Biodiversity: Foundations, Models, Data. Wiley, 2013Crossref Scopus (61) Google Scholar, and predator–prey mass ratios [15.Heckmann L. et al.Interactive effects of body-size structure and adaptive foraging on food-web stability.Ecol. Lett. 2012; 15: 243-250Crossref PubMed Scopus (87) Google Scholar]. One should therefore ask: does this mean that consumer behaviour and body plans are fundamentally determined at the ecosystem level? This work was supported by the Natural Environment Research Council (NE/T003510/1). On the Perils of Ignoring Evolution in NetworksSegar et al.Trends in Ecology & EvolutionAugust 24, 2020In BriefHere, we reply to the stimulating comments from Sagoff [1] and Rossberg [2] on Segar et al. [3]. Sagoff posits that species assemblages are largely fortuitous and ephemeral, which thwarts opportunities for coevolutionary processes [4]. Given the dynamic nature of ecological communities, have populations from different interacting species had sufficient time in which to generate selective pressure on each other? As Rossberg points out, in long-lasting and highly intimate bipartite networks, ‘frequent co-occurrence of the two taxa’ is required for evolutionary lockstep between vulnerability (v) and foraging (f) traits. Full-Text PDF