Selectiondriven decreases in species numbers

Frequency-dependent selection and density-dependent selection are also crucial for understanding how selection pressures can decrease the number of species within an ecological community:

• First, in evolutionary game theory - including all evolutionary models based on matrix games or on the replicator equation - a population's density is not usually part of the model, which describes only the frequencies of different types. Without enhancements, these types of model therefore cannot account for any density-dependent selection pressures, or capture selection-driven extinctions during which a population's density drops to zero.

• Second, in optimization approaches of evolution, a constant fitness landscape governs the course and outcome of evolution, and, accordingly, frequency-dependent selection is absent. Again, the density of the evolving population is usually not part of the model. Even when it is, selection-driven extinctions cannot occur, as no acceptable constant fitness function will be maximized when a population goes extinct.

These two limitations explain why, until relatively recently, population extinctions caused by natural selection were rarely modeled. In particular, landmarks of evolutionary theory are based on notions of optimizing selection: this includes Fisher's so-called fundamental theorem of natural selection (Fisher 1930) and Wright's notion of hill climbing on fitness landscapes (Wright 1932, 1967). Also Levins's seminal fitness-set approach to the study of constrained bivariate evolution (Levins 1962, 1968) is based on the assumption that, within a set of feasible phenotypes defined by a trade-off, evolution will maximize a population's fitness. Even the advent of evolutionary game theory (Maynard Smith 1982), with its conceptually most valuable refocusing of attention towards frequency-dependent selection, did not help as such, since, for the sake of simplicity, population densities were usually removed from consideration in such models (for an alternative approach to game dynamics aimed at including densities, see Cressman 1990).

And yet the potential of adaptations to cause the collapse of populations was recognized early on. Haldane (1932) provided a verbal example by considering overtopping growth in plants. Taller trees get more sunlight while casting shade onto their neighbors. As selection thus causes the average tree height to increase, fecundity and carrying capacity decline because more of the tree's energy budget is diverted from seed production to wood production, and the age at maturation increases. Arborescent growth as an evolutionary response to selection for competitive ability can therefore cause the decline of a population's abundance as well as of its intrinsic growth rate, potentially resulting in population extinction. The phenomenon of selection-driven extinction is closely related to Hardin's (1968) tragedy of the commons. In both cases, strategies or traits that benefit the selfish interests of individuals, and that are therefore bound to invade, undermine the overall interests of the evolving population as a whole once these strategies or traits have become common. Such a disconnect between individual interest and population interest can only occur under frequency-dependent selection - under optimizing selection, the two are equivalent. It is thus clear that frequency-dependent selection and density-dependent selection are both necessary for capturing the potential of adaptive evolution in a single species to cause its own extinction.

Processes of selection-driven extinction can come in several forms: • First, evolutionary suicide (Ferriere 2000) is defined as a trait substitution sequence driven by mutation and selection taking a population toward and across a boundary in the population's trait space beyond which the population cannot persist. Once the population's trait values have evolved close enough to this boundary, mutants can invade that are viable as long as the current resident trait value abounds, but that are not viable on their own. When these mutants start to invade the resident population, they initially grow in number. However, once they have become sufficiently abundant, concomitantly reducing the former resident's density, the mutants bring about their own extinction. Webb (2003) refers to such processes of evolutionary suicide as Darwinian extinction.

• Second, adaptation may cause population size to decline gradually through perpetual selection-driven deterioration. Sooner or later, demographic and environmental stochasticity will then cause population extinction. This phenomenon has been dubbed runaway evolution to self-extinction by Matsuda and Abrams (1994a).

• Third, the population collapse abruptly brought about by an invading mutant phenotype may not directly lead to population extinction but only to a substantial reduction in population size (Dercole et al. 2002). Such a collapse will then render the population more susceptible to extinction by stochastic causes and may thus indirectly be responsible for its extinction.

For univariate traits, the normal form for the invasion fitness of mutants with trait values x' in resident populations with trait values x that are close to a critical trait value x* =0 at which evolutionary suicide occurs is simply given by with the corresponding equilibrium abundance

with c > 0. From this we can see that the selection pressure at x* is positive, g(x*) = 1 > 0, so that trait substitutions in x converge to x*, where the evolving population's equilibrium abundance abruptly drops from 1 to 0.

The occurrence here of a discontinuous transition to extinction is not accidental. As has been explained by Gyllenberg and Parvinen (2001), Gyl-lenberg et al. (2002), and Dieckmann and Ferriere (2004), such a catastrophic bifurcation is a strict prerequisite for evolutionary suicide. The reason is that selection pressures at trait values at which a continuous transition to extinction occurs (e. g., through a transcritical bifurcation) always point in the trait direction that increases population size: evolution towards extinction is then impossible. Allee effects, by contrast, provide standard ecological mechanisms for discontinuous transitions to extinction.

The potential ubiquity of selection-driven extinctions is underscored by numerous examples based on the evolutionary dynamics of many different traits, including competitive ability (Matsuda and Abrams 1994a; Gyllenberg and Parvinen 2001; Dercole et al. 2002), anti-predator behavior (Matsuda and Abrams 1994b), sexual traits (Kirkpatrick 1996; Kokko and Brooks 2003), dispersal rates (Gyllenberg et al. 2002), mutualism rates (Ferriere et al. 2002), cannibalistic traits (Dercole and Rinaldi 2002), maturation reaction norms (Ernande et al. 2002), levels of altruism (Le Galliard et al. 2003), and selfing rates (Cheptou 2004). Dieckmann and Ferriere (2004) showed, by examining ecologically explicit multi-locus models, that selection-driven extinction robustly occurs also under sexual inheritance. Relevant overviews of the mathematical and ecological underpinnings of selection-driven extinction have been provided by Webb (2003), Dieckmann and Ferriere (2004), Rankin and Lopez-Sepulcre (2005), and Parvinen (2006).

Also coevolutionary dynamics can cause extinctions. An early treatment, which still excluded the effects of intraspecific frequency-dependent selection, was provided by Roughgarden (1979, 1983). This limitation has been overcome in modern models of coevolutionary dynamics based, for example, on the canonical equation of adaptive dynamics (e.g., Dieckmann et al. 1995, Dieckmann and Law 1996; Law et al. 1997). Also in this multi-species context it is important to distinguish between continuous and discontinuous transitions to extinction. As has been explained above, evolutionary suicide cannot contribute to an evolutionarily driven continuous transition to extinction. Moreover, such continuous extinctions cause mutation-limited phe-notypic evolution in the dwindling species to grind to a halt, since fewer and fewer individuals are around to give birth to the mutant phenotypes that fuel the adaptive process. This stagnation renders the threatened species increasingly defenseless by depriving it of the ability to counteract the injurious evolution of its partner through suitable adaptation of its own. For these two reasons, continuous evolutionary extinctions are driven solely by adaptations in the coevolving partners. By contrast, when a transition to extinction is discontinuous, processes of evolutionary suicide and of coevolutionary forcing may conspire to oust a species from the evolving community.

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