Adaptive speciation theory.docx

1、Adaptive speciation theoryAdaptive speciation theory:a conceptual reviewAbstract：Speciationthe origin of new speciesis the source of the diversity of life. A theory of speciation is essential to link poorly understood macro-evolutionary processes, such as the origin of biodiversity and adaptive radi

2、ation, to well understood micro-evolutionary processes, such as allele frequency change due to natural or sexual selection. An important question is whether, and to what extent, the process of speciation is adaptive, i.e., driven by natural and/or sexual selection. Here, we discuss two main modellin

3、g approaches in adaptive speciation theory. Ecological models of speciation focus on the evolution of ecological differentiation through divergent natural selection. These models can explain the stable coexistence of the resulting daughter species in the face of interspecific competition, but they a

4、re often vague about the evolution of reproductive isolation. Most sexual selection models of speciation focus on the diversification of mating strategies through divergent sexual selection. These models can explain the evolution of prezygotic reproductive isolation, but they are typically vague on

5、questions like ecological coexistence. By means of an integrated model, incorporating both ecological interactions and sexual selection, we demonstrate that disruptive selection on both ecological and mating strategies is necessary, but not sufficient, for speciation to occur. To achieve speciation,

6、 mating must at least partly reflect ecological characteristics. The interaction of natural and sexual selection is also pivotal in a model where sexual selection facilitates ecological speciation even in the absence of diverging female preferences. In view of these results, it is counterproductive

7、to consider ecological and sexual selection models as contrasting and incompatible views on speciation, one being dominant over the other. Instead, an integrative perspective is needed to achieve a thorough and coherent understanding of adaptive speciation.Keywords: Speciation models . Prezygotic is

8、olation .Postzygotic isolation . Reinforcement . Disruptive selection . Evolutionary branching . Competitive speciation . Sexual selection . Fisherian runaway process . Good-genes models . Condition-dependent ornamentIntroduction:Recently, the scientific world celebrated the 150th anniversary of the

9、 release of Charles Darwins seminal book On the Origin of Species by Natural Selection. Darwins ideas (Darwin 1859;Darwin 1871) on natural and sexual selection have inspired generations of biologists, and we have now a fairly good comprehension of how selection acts within populations and how popula

10、tions are transformed under the influence of selection pressures. It is important to realise, however, that much of our understanding of selection-induced changes relates to the process of anagenesis, the gradual evolution of whole populations. A similar understanding of the role of selection in cla

11、dogenesis, the splitting of species into reproductively isolated units, is largely lacking. Despite of its title, the Origin did actually not contribute much to resolving the question whether andhow speciation is driven by natural selection. A sound understanding of speciation is of key importance f

12、or evolutionary theory, since the birth of new species is the crucial link between micro-evolution (that mainly occurs at or below the species level) and macro-evolutionary processes like adaptive radiations that largely occur above the species level. If speciation tends to be adaptive, that is, dri

13、ven by directional forces like natural or sexual selection, then onecould hope for achieving an overarching adaptive theory including both micro- and macro-evolution. Darwin (Origin, chapter 4) envisaged speciation as the result of two processes: selection for diversification allowing the exploitati

14、on of previously unused opportunities, and the extinction of intermediate forms as a consequence of severe competition among these forms. Hence, according to Darwin, selection plays a major role in the speciation process. In fact, his view comes close to modern ideas on competitive speciation to be

15、discussed below. However, Darwins verbal arguments are often vague and not always convincing, partly because of his pre-Mendelian ideas on inheritance. It is partly for this reason that the founding fathers of the Modern Synthesis largely discarded Darwins view on speciation (Mayr and Provine 1998),

16、 giving nonselective factors like geographic isolation a much more prominent role than selection.Ever since Darwin, theoretical arguments have played an important role in debates on the causes of speciation. In the second half of the 20th century, more than 100 mathematical models have been develope

17、d to study the role of selection in speciation with gene flow (reviewed in Kirkpatrick and Ravign 2002). Although many of these models demonstrate that selection-driven speciation is possible in principle, they typically lead to the conclusion that selection-driven speciation will only occur under h

18、ighly specific conditions or for rather extreme parameter combinations (Felsenstein 1981). Accordingly, speciation models seemed to suggest that adaptive speciation is a rare and unlikely phenomenon. This conclusion is challenged by two recent developments in speciation theory, which seem to suggest

19、 that natural and sexual selection can be more powerful in the creation of new species than the traditional models seem to suggest. First, a variety of ecological speciation models has been developed (Dieckmann et al.2004) that show that Darwins intuitive notion of competitive speciation can be give

20、n a theoretical underpinning. These models are based on a dynamic view of natural selection, allowing selection to switch from stabilising to disruptive in the same coherent framework. The realisation that Darwinian fitness is highly context dependent and dynamic, and that in a diversity of settings

21、, natural selection can drive a population toward a regime of ongoing disruptive selection, makes selection-driven speciation more plausible than in traditional models. Second, various sexual selection models of speciation (Ritchie 2007) give disruptive sexual selection a prominent place in the spec

22、iation process. Several studies (e.g., Turner and Burrows 1995; Higashi et al. 1999) demonstrate that, under specific circumstances, sexual selection may lead to the divergence of female preferences within a single population, eventually leading to reproductive isolation.Both developments have initi

23、ated a fierce debate in the scientific literature. Models of speciation driven by disruptive selection are inherently complex and therefore have to make many simplifying assumptions. The question therefore arises whether the results of these models are general and representative for real-world syste

24、ms, or whether instead, they mainly reflect modelling details or the choice of parameters and initial conditions. In case of ecological speciation models, the analysis is often based on concepts of adaptive dynamics theory, which have been heavily criticised (e.g., Waxman and Gavrilets 2005) and def

25、ended (e.g., Doebeli and Dieckmann 2005). The representativeness of simulation models of ecological speciation have been questioned (e.g., Gavrilets 2004; but see Doebeli and Dieckmann2005) because of their assumptions on the genetic architecture of traits, their choice of parameters like mutation r

26、ate or population size, and their assumptions underlying the evolution of assortative mating (Matessi et al. 2001). Likewise, models of speciation through disruptive sexual selection have been criticised (e.g., Van Doorn and Weissing 2001; Arnegard and Kondrashov 2004;Van Doorn et al. 2004) because

27、of their highly special initial conditions and the lack of stability of the incipient species in the face of ecological competition. For non-specialists (and not only for them!), it is increasingly difficult to judge the scope and validity of the arguments and counterarguments in this debate. This i

28、s partly a consequence of the high degree of technical sophistication required for setting up and analysing adaptive speciation models.Moreover, proponents and opponents tend to base their views on model variants that differ to such an extent in their assumptions that the model outcomes are not dire

29、ctly comparable.In situations like these, it is often impossible to say that one model variant is “inherently” better than an alternative one. Selection-driven speciation results from the intricate interplay of processes at the phenotypic level (where natural and sexual selection are operating) and

30、at the genetic level (where, for example, linkage disequilibria have to evolve between ecological and mating characters), and models focusing simultaneously on both levels tend to be intractable. The more traditional speciation models tend to have their focus on genetic processes and are often quite

31、 sophisticated in this respect. On the downside, they often make simplistic assumptions on selection and mating, which cannot easily be given a mechanistic interpretation and which typically lack a population dynamical underpinning. In contrast, the adaptive dynamics school tends to derive fitness f

32、rom first principles; fitness “emerges” from mechanistic and population dynamical considerations (Metz 2008). On the downside, the assumptions on the underlying genetics are often simplistic and unrealistic. It is important to realise that both approaches have their virtues and their shortcomings; a

33、nd that each approach sheds light on different aspects of the process of speciation. Although the diversity of models and model outcomes may look confusing, a pluralistic approach may actually be the best research strategy for achieving robust insights. Speciation theory is the prototype example of a research field where scientific truth can only be approached t