In a somewhat related phylogenetic approach, several studies report the highest rates of lineage accumulation early in some radiations Burbrink and Pyron ; Phillimore and Price , a pattern consistent with high initial levels of ecological opportunity, followed by declining levels as ecological space fills.
Although suggestive, caution is warranted when using phylogenetic studies alone to infer complex evolutionary mechanisms Losos Ideally, mechanisms by which ecological opportunity shapes development of biological diversity would be evaluated experimentally, and experimental diversification studies in microbes offer substantial insight into the action of ecological opportunity in low-diversity communities. In their landmark study, Rainey and Travisano demonstrated that, when introduced into static broth media, Pseudomonas fluorescens predictably diversifies into three primary ecophenotypic forms, the ancestral broth-adapted smooth form, the wrinkly spreader which forms a surface mat that allows it to capitalize on surface oxygen, and the fuzzy spreader that occupies the anoxic bottom region.
Recently, Thibert-Plante and Gavrilets studied a series of models of ecological speciation with multiple types of phenotypic traits which can be used for mating decisions. Supplier out of stock. Some predictions can be made using well-established theory. What makes this process extremely complex and difficult to understand from the theoretical point of view is that different evolutionary factors controlling the dynamics of speciation such as mutation, random genetic drift, recombination, natural selection, and sexual selection act simultaneously and often have opposite effects. Receive exclusive offers and updates from Oxford Academic. Evolution of flightlessness in rails Gruiformes: Rallidae : phylogenetic, ecomorphological and ontogenetic perspectives. Svensson EI.
This divergent evolution is driven by competition for resources and the associated fitness trade-offs arising from niche adaptation. Evolution of ecophenotypic forms is fully dependent on the ecological opportunity provided by a static medium, as no diversification occurs if the environment is made ecologically homogeneous by continual stirring. Collectively, microbial evolution studies have experimentally verified fundamental mechanisms by which ecological opportunity causes adaptive diversification Kassen Replicate adaptive radiations in the wild also yield evidence for high levels of ecological opportunity in depauperate communities, and moreover, point to a strong element of determinism in the action of ecological opportunity Baldwin ; Gillespie ; Losos Replicate adaptive radiations that are themselves replicated across multiple distinct clades in response to the same ecological factors provide particularly strong evidence that diversification is driven by ecological opportunity in a more or less deterministic process.
Fishes of geologically young postglacial lakes in the Northern Hemisphere provide an example. Two phenotypic forms of European whitefish, Coregonus lavaretus , often occur in northern European lakes, and these pelagic-feeding and benthic-feeding forms are associated with distinct niches. Similar patterns of independent parallel evolution of benthic and pelagic morphs are observed in other salmonids, including North American whitefish, C. Of course, replicate radiations in similar environments are not inevitable Losos , but the several remarkable examples across a diversity of taxa underscore the manifest influence of ecological opportunity in shaping the form of biological diversity in low-diversity communities.
The extent and character of ecological opportunity in species-rich communities is far from clear. Although ecological opportunity is often assumed to decline as communities become more species rich, recent critical evaluation of this assumption suggests unequivocal support is lacking Benton and Emerson ; Losos Thus, increasing species richness may fill previously available niches, but create new ones at the same time.
leondumoulin.nl/language/fiction/i-love-your-smile.php Ecological models of community assembly offer support for a reduction in ecological opportunity as communities accumulate species Grover ; Leibold ; McPeek These analyses suggest that although the number of unfilled niches may remain high in species-rich communities, niche availability declines in the sense that available niches become more restrictive with respect to traits required for a new phenotype to become established and that niche discordance is constrained by narrower niche breadth.
Further species additions are also possible in the community, suggesting that niche space remains available, but as species accumulate in communities, traits of new species must meet ever more stringent phenotypic criteria Grover ; Leibold ; McPeek This narrowing window of niche availability for each additional species implies limited niche discordance due to ecologically constrained postcolonization niche evolution, and thus yields more restricted ecological opportunity.
Although community theory suggests species-rich communities harbor reduced ecological opportunity, natural communities are typically more complex than those captured in community models. Schemske compellingly argued that latitudinal differences in relative importance of abiotic versus coevolutionary drivers of adaptation may contribute significantly to the much higher diversity of tropical communities compared to those of temperate regions.
In abiotically benign tropical communities, continuous reciprocal adaptation in a web of coevolutionary interactions ensures that adaptive niche evolution is ongoing on an ever-fluid adaptive landscape. In temperate communities, by contrast, adaptation to harsh but predictable abiotic conditions primarily drives niche evolution to an optimal phenotype, a stationary adaptive peak.
A colonizing subpopulation may successfully invade a species-rich community because its phenotype is already well adapted to the community high niche availability , but promptly diverge from the source population because niche evolution is ongoing among species high niche discordance , driving divergence and speciation. Additional mechanisms may also operate to create ecological opportunity in species-rich communities. Elevated rates of coevolution in species-rich communities create more opportunities for cospeciation and evolution of more specialized phenotypes, essentially creating niches by more finely dividing ecological space Armbruster and Muchhala Additionally, it may be wrong to assume that niche shifts are more difficult in species-rich communities than in depauperate communities.
Clearly, much remains to be learned about ecological opportunity's role in the buildup of biological diversity in species-rich communities. We anticipate investigations of diversification in species-rich communities will provide new insight into the operation and importance of ecological opportunity in generating biological diversity. One challenge will be to reconcile, through theory and empiricism, the evidence for exhaustion of ecological opportunity with increasing species richness in simple model communities with seemingly high levels available in species-rich communities.
While further theoretical work is needed, ecological opportunity should generally increase following large, rapid, and multifarious environmental shifts — like the changes that commonly result from human activities. Human-induced rapid environmental change HIREC can cause a variety of changes to ecological communities that can influence ecological opportunity, such as:. Not only may HIREC dramatically alter environmental conditions that affect ecological opportunity, but it may also modify factors that influence population responses to ecological opportunity. HIREC likely frequently alters the spatiotemporal structure of ecological opportunity, for instance by changing connectedness among populations e.
Thus, the environmental changes wrought by humans can clearly have major ecological and evolutionary consequences; but might these environmental changes generate both extensive ecological opportunity and adaptive diversification? Because many of the ways that humans alter the environment should result in new niche availability and niche discordance, we suggest that HIREC likely increases ecological opportunity in many cases.
However, considering that until recently little work had investigated the potential diversifying force of HIREC, we currently have inadequate data to assess whether HIREC will eventually produce more extinction than diversification or vice versa. The idea that HIREC may drive widespread patterns of diversification may seem counter to the ample evidence for biotic homogenization, the increased genetic, taxonomic, or functional similarity of biotas over time resulting from species extinctions and invasions McKinney and Lockwood ; Olden ; Rahel But perhaps the occurrence of biotic homogenization indicates that human activities often create similar types of new niche availability within altered communities.
If so, some of the new niche availability may most rapidly be colonized by species with high dispersal abilities that experience little niche discordance because their mean phenotypes already reside near the newly created adaptive peaks in human-altered communities e. Meanwhile, occupancy of additional niche availability created by HIREC, for which most residents or colonizers experience strong niche discordance, may require longer time intervals for establishment and adaptation.
Moreover, the many documented cases of rapid phenotypic shifts subsequent to anthropogenic environmental impacts appear to represent repeated responses to human-created ecological opportunity. If human-modified environments usually generate similar types of new ecological opportunity, and various species adapt to these repeated instances of new adaptive peaks, then this could result in functional homogenization across many localities through a process of contemporary adaptation.
Indeed, many species may currently be in the process of diverging between subpopulations adapted to human-altered environments and ancestral subpopulations less impacted by human activities or affected by different human impacts. We know that divergent natural selection often drives the evolution of reproductive isolation Langerhans and Riesch ; Nosil ; Schluter , we now need focused investigation of how HIREC might generate ecological opportunity and facilitate speciation.
Dynamics of ecologically mediated diversification depend critically on the spatial context in which diversification unfolds Doebeli and Dieckmann ; Emerson and Gillespie ; Urban The spatial structure of ecological opportunity defines the spatial distribution of form, direction, and intensity of selection, and prescribes the scope of spatial opportunities for speciation, primarily through impacts on gene flow Kisel and Barraclough Although niche availability and niche discordance are necessary for diversification under ecological opportunity, these will result in speciation and adaptive radiation only under appropriate spatial and temporal conditions.
Illustrative of this point is Lack's insight into the role of spatial structure in accounting for both the pronounced radiation of Darwin's finches among islands of the Galapagos archipelago where at least 13 species have formed and multiple species coexist on individual islands, and the complete absence of species diversification in the closely related Cocos finch Pinaroloxias inornata inhabiting the isolated and solitary island of Cocos. Lack , p. The Cocos finch has apparently increased phenotypic variance primarily through plasticity of feeding behaviors via learning rather than through evolution of ecotypes or speciation Werner and Sherry Existence of multiple islands in the Galapagos, however, provides the possibility for dispersing individuals to adaptively diverge from the source population unimpeded by gene flow.
Lack's explanation has stood the test of time Grant and Grant , and archipelagos in general provide spatial opportunity for divergence and speciation in birds Kisel and Barraclough Temporal processes are implicit in Lack's explanation, first because ecological differences in allopatry must be sufficiently stable over time that divergence occurs and is maintained, and second because divergence in isolation must be sustained for a sufficient duration that accumulated phenotypic and genetic differences are not lost to hybridization upon secondary contact.
Spatial distribution of ecological opportunity impacts diversification by shaping patterns of gene flow between subpopulations, which in turn establishes dynamics of response to divergent selection and likelihood of speciation. Divergent selection may occur between geographically isolated populations at one extreme, or among spatially intermixed mosaics at the other, with intermediate spatial structures formed by spatially continuous populations distributed along gradual or abrupt ecological gradients.
Dynamics of divergence and speciation differ across this spectrum of geographic arrangements Bolnick and Fitzpatrick ; Coyne and Orr While allopatric speciation can occur by nonecological mechanisms, theory and empirical evidence suggest that ecological opportunity plays a prominent role in many, perhaps most, cases Schluter ; Langerhans and Riesch ; but see Rundell and Price Spatial ecological gradients and discontinuities also may produce divergent selection that leads to speciation, but strong divergent selection may be required to overcome genetic mixing across the gradient or discontinuity Via In the absence of additional mechanisms driving completion of speciation, such as reinforcement, sexual selection, or genetic opportunities for speciation Feder and Nosil ; Hoffman and Rieseberg ; Ritchie , divergent ecotypes might persist indefinitely under a selection-migration balance.
Ecological opportunity provides an environmental substrate conducive to diversification, but its evolutionary consequences depend on characteristics of populations that experience the environment. The concept of diversification potential has long been integral in discussions of ecological opportunity Mayr , and previous work reviewing topics such as traits associated with among-clade variation in speciation rates Coyne and Orr ; Jablonski have generally indicated that diversification potential varies among populations, species, and clades.
Diversification potential refers to the properties of a population that influence its potential to encounter and respond to ecological opportunity. While phenotypic and lineage diversification can occur in the absence of ecological opportunity, such as through genetic drift, nonecological sources of sexual selection, and differential responses to similar selection pressures see Langerhans and Riesch , we more narrowly restrict diversification potential to refer specifically to the context of diversifying selection caused by ecological opportunity.
Diversification potential comprises three components E : probability that ecological opportunity of a magnitude sufficient to potentially cause speciation is encountered by a population. V : probability that phenotypic variance of ecological traits increases following the encounter with ecological opportunity. I : probability that reproductive isolation evolves following increased phenotypic variance. E : A variety of factors impact the probability of encountering ecological opportunity, including dispersal, persistence, phenotypic variability, and niche construction.
Higher dispersal frequency allows greater sampling of habitats within the dispersal range, and greater dispersal range increases the spatial scope of habitats encountered, and both affect probability of colonizing ecologically novel habitats Kisel and Barraclough ; MacArthur and Wilson Population phenotypic variability enhances diversification potential because more variable populations may encounter a greater scope of niche availability in the environment, such as experiencing additional adaptive peaks far from the population mean.
V : Population characteristics that increase V include any attribute that facilitates phenotypic evolution in response to natural selection. Magnitude and form of response to selection depends on many factors, including selection intensity, degree and form of genetic co variances of traits in a population, level of gene flow between diverging subpopulations, pleiotropic effects, and effective population size Hartl and Clark Empirical studies of response to selection on a focal trait often find agreement with simple quantitative models Galen ; Grant and Grant , but genetic architecture and fitness tradeoffs among traits may add substantial complexity to a population's response to selection Kirkpatrick ; Schluter Three particular characteristics — limited dispersal, sexual selection, and genetic mechanisms —may be especially influential.
Traits associated with restricted dispersal of individuals between diverging populations may give rise to evolution of reproductive isolation by reducing rates of recombination Felsenstein ; Nosil , and dispersal distance is closely associated with spatial scale of speciation across taxa on islands Kisel and Barraclough However, elevated dispersal may not always hinder progress toward speciation. Dispersal may additionally induce completion of speciation by initiating the process of reinforcement Servedio ; Servedio and Kirkpatrick Because sexual selection acts directly on traits involved in reproduction, it may advance completion of speciation, and may prove most effective in driving speciation when it occurs in concert with divergent natural selection Coyne and Orr ; Ritchie ; but see Maan and Seehausen Some groups may fail to diversify because one probability is low, despite high values of the other two parameters.
For example, spatially divided populations of Trinidadian guppies, Poecilia reticulata experience divergent natural selection imposed by alternative regimes of predation, and readily diverge in ecological traits, but do not evolve reproductive isolation Magurran Although E , V , and I may each limit rates of diversification in specific lineages or ecological conditions, we generally have only idiosyncratic knowledge of how relative values of these probabilities vary across taxa and environments, and whether one probability overwhelmingly constrains diversification.
Key innovations cause elevated diversification rates through increases in any combination of E , V , or I. For instance, the evolution of wings capable of flight in birds, bats, and pterosaurs may have dramatically increased E ; the decoupling of pharyngeal and oral jaws in cichlid fishes may have greatly enhanced V ; and complex communication structures in birds syrinx and frogs ear papillae may have strengthened I. Although their identification and study presents conceptual and empirical challenges Donoghue , novel traits linked with increased E , V , or I appear associated with many radiations, and may underlie the most dramatic radiations in the history of life.
Ecological opportunity has formed the core of our ideas for the evolution and buildup of biological diversity since Darwin's description of the basic concept in On the Origin of Species , yet we have lacked a comprehensive framework for elucidating its scope, action, and consequences. Our goal has been to provide greater clarity to the concept of ecological opportunity by defining its fundamental elements, and we hope this exposition motivates more focused theoretical and empirical development. Much work remains. A central obstacle to a deeper understanding of the role of ecological opportunity in shaping the diversity of life is development of predictive approaches to its action.
Despite the substantial conceptual importance of ecological opportunity, apparent from the concept's longstanding utility in evolutionary biology, it has so far lacked a predictive framework Losos Such a framework may allow us to understand, for example, why adaptive radiations occur in some cases or habitats but not others.
The obvious path to a predictive framework involves quantification and integration of niche availability, niche discordance, spatiotemporal structure of ecological opportunity, and diversification potential, all of which have been quantitatively examined individually in various ways e. A stumbling block to unification of these elements, however, is the disparate approaches and metrics inherent in each component.
Nonetheless, innovative methods for integration of components will likely be rewarded with significant new applications and insights that will illuminate details of how ecological opportunity shapes biological diversity. Ecological opportunity lies at the intersection of community ecology and evolutionary biology, and advances in our understanding of adaptive diversification will benefit most from explicit synthesis of these disciplines.
Are niche availability and niche discordance often positively or negatively associated in nature, and what conditions influence these associations? We need to understand how properties of ecological opportunity, its spatiotemporal structure, and diversification potential impact the scale of diversification.