- Email: [email protected]
The founder space race: a reply to Buckley et al.
Letters effects’ to describe how genetic structure within newly colonised areas impedes establishment of invading taxa misrepresents the process and does not address all the main mechanisms by which this can occur. The arrival of a taxon in an area can be broken down into three phases: (i) dispersal; (ii) colonisation; and (iii) establishment. Dispersal occurs when individuals or propagules arrive in an area. Colonisation occurs when propagules grow and/or individuals survive long enough to breed. For establishment, the new population must overcome obstacles to expansion, such as strong Allee effects, and expand to a point where it is self-replacing. The ‘founder takes all’ principle, as referred to by Waters et al. [1], is primarily concerned with establishment. Although several taxa may enter the dispersal and/or colonisation phases in an area, it is not until establishment occurs that evolutionary patterns begin to form. The main mechanism that Waters et al. invoke for the generation of genetic structure could otherwise be called ‘space pre-emption’ [2], where different taxa dominate different parts of a newly occupied range, simply due to variation in arrival order. This process of differential space pre-emption leading to genetic structuring is a ‘priority effect’. Priority effects occur where there are intertaxon interactions whose outcome depends on the relative or absolute timing of arrival of the interacting taxa [3]. This allows for different establishment outcomes for taxa in similar areas, even with the same potential taxon pool. Priority effects are not, as implied by Waters et al. [1], density dependent. Density-dependent processes are those that change with an increase in population density, such as density-dependent competition [4]. Although the occupancy of space depends on the density of the resident population, the order or arrival of taxa depends on their dispersal characteristics and chance events, rather than on the density of the resident population. We argue that evolutionary biologists and ecologists should consider several additional, not mutually exclusive, mechanisms that maintain genetic structuring within populations. First, pre-existing variation, including behavioural variation, such as social behaviour and differing
Trends in Ecology & Evolution April 2013, Vol. 28, No. 4
dispersal ability, may provide particular taxa with a competitive advantage that could be considered a preadaptation for establishment. Second, niche specialisation of established taxa could exclude invaders because these resident individuals perform better in their new environment due to local adaptation, biasing the outcomes of competitive interactions. Third, genetic incompatibility or assortative mating may exclude invaders because their propagules do not produce fertile offspring. Fourth, temporal effects occur when there has been insufficient time for genetic heterogeneity to arise due to the rarity of colonisation events (i.e., number of colonisations and success of interbreeding) relative to the length of time required for genetic material from invading taxa to become detectable. These processes are not necessarily density dependent. For example, niche specialisation could be density independent because the success of the established taxon depends on its relative fitness advantage in the local environment, rather than on its density. Ultimately, what is of interest in this discussion is how these ecological mechanisms scale with time, from a few generations to hundreds of thousands of years. Over longer timescales, changes in multiple ecological processes and environments are likely to occur. Conclusions about ecological causes of evolutionary patterns must be made with care to ensure that such complexities are accounted for. Opening a dialogue between ecologists and evolutionary biologists is a useful start. References 1 Waters, J.M. et al. (2013) Founder takes all. Density-dependent processes structure biodiversity. Trends Ecol. Evol. 28, 78–85 2 Connolly, S.R. and Muko, S. (2003) Space pre-emption, size-dependent competition and the coexistence of clonal growth forms. Ecology 84, 2979–2988 3 Lawler, S.P. and Morin, P.J. (1993) Temporal overlap, competition, and priority effects in larval anurans. Ecology 74, 174–182 4 Begon, M. et al. (1996) Ecology: Individuals, Populations and communities, Blackwell Scientific Publications 0169-5347/$ – see front matter ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tree.2013.01.005 Trends in Ecology & Evolution, April 2013, Vol. 28, No. 4
The founder space race: a reply to Buckley et al. Jonathan M. Waters1, Ceridwen I. Fraser2, Samuel C. Banks2, and Godfrey M. Hewitt3 1
Allan Wilson Centre for Molecular Ecology and Evolution, Department of Zoology, University of Otago, 340 Great King Street, Dunedin 9016, New Zealand 2 Fenner School of Environment and Society, Australian National University, Building 48, Linnaeus Way, Canberra, ACT 0200, Australia 3 School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, UK
We are delighted that Buckley and co-authors [1] share our interest in the long-term legacy of priority effects, and their reply to our article [2] raises several interesting discussion points. Our synthesis sought to highlight the broad conceptual links and similarities between diverse examples of Corresponding author: Waters, J.M. ([email protected]).
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density-dependent competitive exclusion of late arrivals by founders (‘founder takes all’) over a wide range of temporal and spatial scales. Naturally, with such a broad scope, the many various ecological factors that can influence the strength of such density-dependent processes could not be fully discussed, but we welcome an opportunity to extend our synthesis via this conversation.
Letters Unfortunately, we feel that Buckley et al.’s response [1] focuses too much on semantics. Their criticism of our use of the term ‘density-dependent processes’ is, we feel, both unfounded and of little importance to the broader concepts under consideration. We used the term ‘density dependent’ to encapsulate diverse priority-effect processes, such as gene surfing, competitive exclusion, and density blocking. Buckley et al. argue that such processes do not depend on density. Although the term ‘density’ is often absent from standard ecological definitions of ‘priority effects’, there is strong evidence that density is indeed a key player that underpins and links such processes (e.g., [3,4]). In most cases, priority effects are driven largely by competitive exclusion, which is very much a density-dependent phenomenon (density being relative to resource availability). As a case in point, a small (low-density) population of the prehistoric penguin Megadyptes waitaha, no matter how well adapted to mainland New Zealand, could not have so successfully excluded the sub-Antarctic species Megadyptes antipodes [5]. Additionally, despite Buckley et al.’s [1] contention that priority effects are strictly an intertaxon phenomenon, this is not the case (e.g., [3,4,6]); and our article [2] provides numerous additional intraspecific examples to counter this rather too narrow view. Indeed, one of the goals of our article was to highlight the numerous examples of intraspecific priority effects that genetic data have revealed. More generally, we feel that major conceptual advances often rely on broad consideration of concepts (e.g., recognition that short-term intraspecific ecological and genetic processes can be linked to broader, long-term ecological and evolutionary phenomena). We wholeheartedly agree with Buckley et al.’s [1] call for increased dialogue between ecologists and evolutionary biologists. We also agree with the uncontroversial suggestion that numerous different biological processes can po-
Trends in Ecology & Evolution April 2013, Vol. 28, No. 4
tentially promote population genetic structure, and could influence the strength and direction of priority effects. Indeed, Buckley et al.’s point that niche specialisation of an established taxon can perhaps bias competitive interactions, echoes De Meester’s [7] Monopolisation Hypothesis; that is, that first colonisers have a head start on local adaptation. Nonetheless, we argue that many priority effects cannot be explained by local adaptation and niche pre-emption; for example, in long-lasting patterns of postglacial recolonisation, the dense and broadly distributed recolonised lineages (e.g., European hedgehogs [8] or southern bull-kelp [9]) are also found in source populations elsewhere. References 1 Buckley, H.L. et al. (2013) The founder space race: a response to Waters et al. Trends Ecol. Evol. 28, 189–190 2 Waters, J.M. et al. (2012) Founder takes all: density-dependent processes structure biodiversity. Trends Ecol. Evol. 28, 78–85 3 Tupper, M. and Boutilier, R.G. (1995) Effects of conspecific density on settlement, growth and postsettlement survival of a temperate reef fish. J. Exp. Mar. Biol. Ecol. 191, 209–222 4 Eitam, A. et al. (2005) Density and intercohort priority effects on larval Salamandra salamandra in temporary pools. Oecologia 146, 36–42 5 Boessenkool, S. et al. (2009) Relict or colonizer? Extinction and range expansion of penguins in southern New Zealand. Proc. R. Soc. B 276, 815–821 6 Almany, G.R. (2003) Priority effects in coral reef fish communities. Ecology 84, 1920–1935 7 De Meester, L. et al. (2002) The Monopolization Hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecol. 23, 121–135 8 Seddon, J.M. et al. (2001) DNA footprints of European hedgehogs, Erinaceus europaeus and E. concolor: Pleistocene refugia, postglacial expansion and colonization routes. Mol. Ecol. 10, 2187–2198 9 Fraser, C.I. et al. (2009) Kelp genes reveal effects of subantarctic sea ice during the Last Glacial Maximum. Proc. Natl. Acad. Sci. U.S.A. 106, 3249–3253 0169-5347/$ – see front matter ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tree.2013.01.008 Trends in Ecology & Evolution, April 2013, Vol. 28, No. 4
‘Niche’ or ‘distribution’ modelling? A response to Warren Greg J. McInerny1,2 and Rampal S. Etienne3 1
Department of Computer Science, University of Oxford, Oxford OX1 3QD, UK Computational Ecology and Environmental Science Group, Computational Science Laboratory, Microsoft Research, Cambridge CB3 0FB, UK 3 Community and Conservation Ecology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, 9700 CC Groningen, The Netherlands 2
Recently, Warren [1] argued that correlative modelling of species distribution and environmental data should be described as Ecological Niche Modelling (ENM) rather than Species Distribution Modelling (SDM). Although discussions of terminology could be posed as semantics and nit-picking, they are symptomatic of deeper challenges to robustly define the philosophy, methodology, and theory of Corresponding author: McInerny, G.J. ([email protected]).
this science. Terminology should standardise definitions and facilitate understanding and communication, while enabling synthesis and innovation. Thus, we agree with Warren’s appeal for greater clarity. However, we argue that ‘niche’ is confusing and impedes progress. By contrast we argue that SDM is better positioned to promote much needed clarity and innovation. Warren implies that ‘niche’ is somehow unique in linking survival, reproduction, and existence to environmental 191
Trends in Ecology & Evolution April 2013, Vol. 28, No. 4
dispersal ability, may provide particular taxa with a competitive advantage that could be considered a preadaptation for establishment. Second, niche specialisation of established taxa could exclude invaders because these resident individuals perform better in their new environment due to local adaptation, biasing the outcomes of competitive interactions. Third, genetic incompatibility or assortative mating may exclude invaders because their propagules do not produce fertile offspring. Fourth, temporal effects occur when there has been insufficient time for genetic heterogeneity to arise due to the rarity of colonisation events (i.e., number of colonisations and success of interbreeding) relative to the length of time required for genetic material from invading taxa to become detectable. These processes are not necessarily density dependent. For example, niche specialisation could be density independent because the success of the established taxon depends on its relative fitness advantage in the local environment, rather than on its density. Ultimately, what is of interest in this discussion is how these ecological mechanisms scale with time, from a few generations to hundreds of thousands of years. Over longer timescales, changes in multiple ecological processes and environments are likely to occur. Conclusions about ecological causes of evolutionary patterns must be made with care to ensure that such complexities are accounted for. Opening a dialogue between ecologists and evolutionary biologists is a useful start. References 1 Waters, J.M. et al. (2013) Founder takes all. Density-dependent processes structure biodiversity. Trends Ecol. Evol. 28, 78–85 2 Connolly, S.R. and Muko, S. (2003) Space pre-emption, size-dependent competition and the coexistence of clonal growth forms. Ecology 84, 2979–2988 3 Lawler, S.P. and Morin, P.J. (1993) Temporal overlap, competition, and priority effects in larval anurans. Ecology 74, 174–182 4 Begon, M. et al. (1996) Ecology: Individuals, Populations and communities, Blackwell Scientific Publications 0169-5347/$ – see front matter ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tree.2013.01.005 Trends in Ecology & Evolution, April 2013, Vol. 28, No. 4
The founder space race: a reply to Buckley et al. Jonathan M. Waters1, Ceridwen I. Fraser2, Samuel C. Banks2, and Godfrey M. Hewitt3 1
Allan Wilson Centre for Molecular Ecology and Evolution, Department of Zoology, University of Otago, 340 Great King Street, Dunedin 9016, New Zealand 2 Fenner School of Environment and Society, Australian National University, Building 48, Linnaeus Way, Canberra, ACT 0200, Australia 3 School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, UK
We are delighted that Buckley and co-authors [1] share our interest in the long-term legacy of priority effects, and their reply to our article [2] raises several interesting discussion points. Our synthesis sought to highlight the broad conceptual links and similarities between diverse examples of Corresponding author: Waters, J.M. ([email protected]).
190
density-dependent competitive exclusion of late arrivals by founders (‘founder takes all’) over a wide range of temporal and spatial scales. Naturally, with such a broad scope, the many various ecological factors that can influence the strength of such density-dependent processes could not be fully discussed, but we welcome an opportunity to extend our synthesis via this conversation.
Letters Unfortunately, we feel that Buckley et al.’s response [1] focuses too much on semantics. Their criticism of our use of the term ‘density-dependent processes’ is, we feel, both unfounded and of little importance to the broader concepts under consideration. We used the term ‘density dependent’ to encapsulate diverse priority-effect processes, such as gene surfing, competitive exclusion, and density blocking. Buckley et al. argue that such processes do not depend on density. Although the term ‘density’ is often absent from standard ecological definitions of ‘priority effects’, there is strong evidence that density is indeed a key player that underpins and links such processes (e.g., [3,4]). In most cases, priority effects are driven largely by competitive exclusion, which is very much a density-dependent phenomenon (density being relative to resource availability). As a case in point, a small (low-density) population of the prehistoric penguin Megadyptes waitaha, no matter how well adapted to mainland New Zealand, could not have so successfully excluded the sub-Antarctic species Megadyptes antipodes [5]. Additionally, despite Buckley et al.’s [1] contention that priority effects are strictly an intertaxon phenomenon, this is not the case (e.g., [3,4,6]); and our article [2] provides numerous additional intraspecific examples to counter this rather too narrow view. Indeed, one of the goals of our article was to highlight the numerous examples of intraspecific priority effects that genetic data have revealed. More generally, we feel that major conceptual advances often rely on broad consideration of concepts (e.g., recognition that short-term intraspecific ecological and genetic processes can be linked to broader, long-term ecological and evolutionary phenomena). We wholeheartedly agree with Buckley et al.’s [1] call for increased dialogue between ecologists and evolutionary biologists. We also agree with the uncontroversial suggestion that numerous different biological processes can po-
Trends in Ecology & Evolution April 2013, Vol. 28, No. 4
tentially promote population genetic structure, and could influence the strength and direction of priority effects. Indeed, Buckley et al.’s point that niche specialisation of an established taxon can perhaps bias competitive interactions, echoes De Meester’s [7] Monopolisation Hypothesis; that is, that first colonisers have a head start on local adaptation. Nonetheless, we argue that many priority effects cannot be explained by local adaptation and niche pre-emption; for example, in long-lasting patterns of postglacial recolonisation, the dense and broadly distributed recolonised lineages (e.g., European hedgehogs [8] or southern bull-kelp [9]) are also found in source populations elsewhere. References 1 Buckley, H.L. et al. (2013) The founder space race: a response to Waters et al. Trends Ecol. Evol. 28, 189–190 2 Waters, J.M. et al. (2012) Founder takes all: density-dependent processes structure biodiversity. Trends Ecol. Evol. 28, 78–85 3 Tupper, M. and Boutilier, R.G. (1995) Effects of conspecific density on settlement, growth and postsettlement survival of a temperate reef fish. J. Exp. Mar. Biol. Ecol. 191, 209–222 4 Eitam, A. et al. (2005) Density and intercohort priority effects on larval Salamandra salamandra in temporary pools. Oecologia 146, 36–42 5 Boessenkool, S. et al. (2009) Relict or colonizer? Extinction and range expansion of penguins in southern New Zealand. Proc. R. Soc. B 276, 815–821 6 Almany, G.R. (2003) Priority effects in coral reef fish communities. Ecology 84, 1920–1935 7 De Meester, L. et al. (2002) The Monopolization Hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecol. 23, 121–135 8 Seddon, J.M. et al. (2001) DNA footprints of European hedgehogs, Erinaceus europaeus and E. concolor: Pleistocene refugia, postglacial expansion and colonization routes. Mol. Ecol. 10, 2187–2198 9 Fraser, C.I. et al. (2009) Kelp genes reveal effects of subantarctic sea ice during the Last Glacial Maximum. Proc. Natl. Acad. Sci. U.S.A. 106, 3249–3253 0169-5347/$ – see front matter ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tree.2013.01.008 Trends in Ecology & Evolution, April 2013, Vol. 28, No. 4
‘Niche’ or ‘distribution’ modelling? A response to Warren Greg J. McInerny1,2 and Rampal S. Etienne3 1
Department of Computer Science, University of Oxford, Oxford OX1 3QD, UK Computational Ecology and Environmental Science Group, Computational Science Laboratory, Microsoft Research, Cambridge CB3 0FB, UK 3 Community and Conservation Ecology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, 9700 CC Groningen, The Netherlands 2
Recently, Warren [1] argued that correlative modelling of species distribution and environmental data should be described as Ecological Niche Modelling (ENM) rather than Species Distribution Modelling (SDM). Although discussions of terminology could be posed as semantics and nit-picking, they are symptomatic of deeper challenges to robustly define the philosophy, methodology, and theory of Corresponding author: McInerny, G.J. ([email protected]).
this science. Terminology should standardise definitions and facilitate understanding and communication, while enabling synthesis and innovation. Thus, we agree with Warren’s appeal for greater clarity. However, we argue that ‘niche’ is confusing and impedes progress. By contrast we argue that SDM is better positioned to promote much needed clarity and innovation. Warren implies that ‘niche’ is somehow unique in linking survival, reproduction, and existence to environmental 191