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Ecological Fitting by Phenotypically Flexible Genotypes Ecology Letters, (2008) 11: 1123–1134 doi: 10.1111/j.1461-0248.2008.01237.x IDEA AND PERSPECTIVE Ecological fitting by phenotypically flexible genotypes: implications for species associations, community assembly and evolution Abstract Salvatore J. Agosta* and Ecological fitting is the process whereby organisms colonize and persist in novel Jeffrey A. Klemens environments, use novel resources or form novel associations with other species as a Department of Biology, result of the suites of traits that they carry at the time they encounter the novel condition. University of Pennsylvania, This paper has four major aims. First, we review the original concept of ecological fitting Philadelphia, PA 19014, USA and relate it to the concept of exaptation and current ideas on the positive role of *Correspondence: E-mail: phenotypic plasticity in evolution. Second, we propose phenotypic plasticity, correlated [email protected] trait evolution and phylogenetic conservatism as specific mechanisms behind ecological fitting. Third, we attempt to operationalize the concept of ecological fitting by providing explicit definitions for terms. From these definitions, we propose a simple conceptual model of ecological fitting. Using this model, we demonstrate the differences and similarities between ecological fitting and ecological resource tracking and illustrate the process in the context of species colonizing new areas and forming novel associations with other species. Finally, we discuss how ecological fitting can be both a precursor to evolutionary diversity or maintainer of evolutionary stasis, depending on conditions. We conclude that ecological fitting is an important concept for understanding topics ranging from the assembly of ecological communities and species associations, to biological invasions, to the evolution of biodiversity. Keywords Adaptation, biogeography, biological invasion, climate change, community ecology, exaptation, fitness space, host shift, operative environment, pre-adaptation, resource tracking. Ecology Letters (2008) 11: 1123–1134 The concept of ecological fitting developed within the INTRODUCTION historical context of concerns about what Janzen (1980) Janzen (1985) coined the term Ôecological fittingÕ to describe and others (e.g. Holmes & Price 1980; Brooks 1985) the situation in which an organism interacts with its biotic perceived as the overuse of coevolutionary arguments to and abiotic environment in a way that appears to indicate a explain associations among species (Agosta 2006 and shared evolutionary history, when in fact the organismal references therein). One of JanzenÕs main concerns was traits relevant to the interaction evolved elsewhere and in that, when cases of ecological fitting occur, it will be very response to a different set of environmental conditions. difficult to distinguish them from cases of long-term Ecological fitting was presented as a contrasting view to, coexistence because the essential biological result, coexis- and as an appropriate null hypothesis for, the assumption tence and direct or diffuse interaction, is the same. Without that currently observed associations among organisms are an understanding of ecological fitting, biologists, naive to evidence of shared evolutionary history or, more generally, the true histories of organisms present in a community, as a response to explicitly adaptationist arguments to explain would be encouraged to invent spurious adaptive or the presence of a phenotype or species in a particular coevolutionary scenarios to describe interactions for which environment. they are not needed. Ó 2008 Blackwell Publishing Ltd/CNRS 1124 S. J. Agosta and J. A. Klemens Idea and Perspective Ecological fitting was initially recognized by Janzen establish populations under novel conditions beyond those (1985), and subsequently discussed by Brooks & McLennan conditions encountered in their previous evolutionary (2002), as being closely related to the concept of exaptation history, circumvents adaptive processes to produce novel (Williams 1966; Gould & Vrba 1982). The process by which ecological interactions between organisms and the environ- an existing trait is co-opted for a different function ment. These novel ecological interactions can then provide (exaptation) is fundamentally the same as that by which an novel selective environments (e.g. novel species associa- existing genotype obtains realized fitness in a novel selective tions) on which natural selection can work. environment (ecological fitting). Brooks & McLennan For those familiar with West-EberhardÕs (2003) recent (2002) noted that the frequency with which ecological work, Developmental Plasticity and Evolution, the preceding fitting occurs in nature depends in part on the ability of paragraph should be reminiscent of what some have termed traits to be co-opted for novel functions. Below we will the Ôplasticity theoryÕ of biodiversity (Janz et al. 2006; argue that the process of ecological fitting is essentially the Weingartner et al. 2006; Nylin & Wahlberg 2008). Building process of exaptation taking place on a shorter time scale on a history of ideas on the positive role of phenotypic than that over which it is normally considered. Or, in other plasticity in evolution (e.g. the ÔBaldwin effectÕ: Baldwin words, that ecological fitting is the ecological case of 1896; Robinson & Dukas 1999), West-Eberhard argues (1) exaptation. that genotypes are inherently phenotypically plastic, (2) that Subsequent to Janzen (1985), ecological fitting received this plasticity can allow genotypes (individuals) to obtain little attention in the ecology and evolutionary biology realized fitness under novel environmental conditions and, literature even as the essence of the concept continued to be therefore, (3) that Ô…the origin and evolution of adaptive implied by biologists studying species invasions and novelty do not await mutation; on the contrary, genes are introductions (e.g. Holway et al. 2002; Yeh & Price 2004; followers, not leaders, in evolutionÕ (p. 20). This view has Suarez et al. 2005; Strauss et al. 2006), biogeographers been met with some opposition. de Jong (2005) argues that debating the relative roles of dispersal and colonization vs. West-EberhardÕs (2003) proposed process of genetic assim- vicariance (e.g. Pennington & Dick 2004), and evolutionary ilation– which describes trait evolution resulting from the biologists in discussing adaptation, Ôpre-adaptationÕ and initial exposure of novel phenotypic variants arising from exaptation (see below). The term ecological fitting has developmental plasticity to novel conditions – is (1) not survived, however, and has been used by researchers unique within the Darwinian synthesis if one considers interested in the factors structuring species associations plasticity itself an evolved quantitative genetic trait and (2) (Gill 1987; White & Stiles 1992; Chenuil & McKey 1996; not a major avenue for trait evolution based on current Flowers & Janzen 1997; Yu & Davidson 1997; Brooks & empirical or model support. McLennan 2002; Janzen 2003; Agosta & Janzen 2005; We leave the reader to delve further into these arguments. Agosta 2006; Brooks et al. 2006), whole ecosystems For our purposes, we find the above issues to be largely (Wilkinson 2004) and even the dynamics of emerging immaterial to West-EberhardÕs broader contribution: that infectious diseases (Brooks & Ferrao 2005). Nonetheless, phenotypic plasticity, whether evolved or a developmental there has been little attempt to operationalize the concept of by-product, can allow existing genotypes to obtain fitness ecological fitting and incorporate it into mainstream and therefore persist in novel environments without ecological and evolutionary theory. This is unfortunate awaiting novel mutations, thereby placing existing genotypes because ecological fitting has considerable explanatory into novel selective environments where natural selection power (Brooks & McLennan 2002; Wilkinson 2004; Brooks can potentially act. This is a fundamentally different view of & Ferrao 2005; Agosta 2006; Brooks et al. 2006) and is a phenotypic plasticity compared to its historical role in natural null hypothesis for a range of research programmes evolutionary thought. In this formulation, phenotypic (e.g. any prediction of organismal form or function derived plasticity provides ÔfodderÕ for evolution, rather than being from optimality theory; Agosta 2006). merely the environmental noise that is selected against by However, we argue that ecological fitting has much stabilizing selection or that drags against the efficacy of greater importance than simply acting as a null hypothesis or directional selection (Stearns 1989; Thompson 1991). null explanation in ecology and evolutionary biology. We The connections between recent arguments for a positive argue as did Janzen (1985) that ecological fitting is an role of phenotypic plasticity in evolution (West-Eberhard inevitable and frequent process in nature that results from 1989, 2003; Robinson & Dukas 1999; Gorur 2004; Yeh & the interaction between highly flexible organisms and highly Price 2004; Fordyce 2006; Janz et al. 2006; Weingartner et al. variable biotic and abiotic environments. In what follows, 2006; Nylin & Wahlberg 2008) and JanzenÕs (1985) concept we develop a framework within which to evaluate this of ecological fitting are tangible and ripe for synthesis assertion. We will also show how the process of ecological (Agosta 2006). This paper has four aims. First, we describe fitting, whereby organisms obtain
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