Michael Doebeli

On the origin of species by sympatric speciation

Understanding speciation is a fundamental biological problem. It is believed that many species originated through allopatric divergence, where new species arise from geographically isolated populations of the same ancestral species. In contrast, the possibility of sympatric speciation (in which new species arise without geographical isolation) has often been dismissed, partly because of theoretical difficulties,. Most previous models analysing sympatric speciation concentrated on particular aspects of the problem while neglecting others. Here we present a model that integrates a novel combination of different features and show that sympatric speciation is a likely outcome of competition for resources. We use multilocus genetics to describe sexual reproduction in an individual-based model, and we consider the evolution of assortative mating (where individuals mate preferentially with like individuals) depending either on an ecological character affecting resource use or on a selectively neutral marker trait. In both cases, evolution of assortative mating often leads to reproductive isolation between ecologically diverging subpopulations. When assortative mating depends on a marker trait, and is therefore not directly linked to resource competition, speciation occurs when genetic drift breaks the linkage equilibrium between the marker and the ecological trait. Our theory conforms well with mounting empirical evidence for the sympatric origin of many species.

Spatial structure often inhibits the evolution of cooperation in the snowdrift game

Understanding the emergence of cooperation is a fundamental problem in evolutionary biology. Evolutionary game theory has become a powerful framework with which to investigate this problem. Two simple games have attracted most attention in theoretical and experimental studies: the Prisoners Dilemma and the snowdrift game (also known as the hawk–dove or chicken game). In the Prisoners Dilemma, the non-cooperative state is evolutionarily stable, which has inspired numerous investigations of suitable extensions that enable cooperative behaviour to persist. In particular, on the basis of spatial extensions of the Prisoners Dilemma, it is widely accepted that spatial structure promotes the evolution of cooperation. Here we show that no such general predictions can be made for the effects of spatial structure in the snowdrift game. In unstructured snowdrift games, intermediate levels of cooperation persist. Unexpectedly, spatial structure reduces the proportion of cooperators for a wide range of parameters. In particular, spatial structure eliminates cooperation if the cost-to-benefit ratio of cooperation is high. Our results caution against the common belief that spatial structure is necessarily beneficial for cooperative behaviour.

Speciation along environmental gradients

Traditional discussions of speciation are based on geographical patterns of species ranges. In allopatric speciation, long-term geographical isolation generates reproductively isolated and spatially segregated descendant species. In the absence of geographical barriers, diversification is hindered by gene flow. Yet a growing body of phylogenetic and experimental data suggests that closely related species often occur in sympatry or have adjacent ranges in regions over which environmental changes are gradual and do not prevent gene flow. Theory has identified a variety of evolutionary processes that can result in speciation under sympatric conditions, with some recent advances concentrating on the phenomenon of evolutionary branching. Here we establish a link between geographical patterns and ecological processes of speciation by studying evolutionary branching in spatially structured populations. We show that along an environmental gradient, evolutionary branching can occur much more easily than in non-spatial models. This facilitation is most pronounced for gradients of intermediate slope. Moreover, spatial evolutionary branching readily generates patterns of spatial segregation and abutment between the emerging species. Our results highlight the importance of local processes of adaptive divergence for geographical patterns of speciation, and caution against pitfalls of inferring past speciation processes from present biogeographical patterns.

Evolutionary Branching and Sympatric Speciation Caused by Different Types of Ecological Interactions

Evolutionary branching occurs when frequency‐dependent selection splits a phenotypically monomorphic population into two distinct phenotypic clusters. A prerequisite for evolutionary branching is that directional selection drives the population toward a fitness minimum in phenotype space. This article demonstrates that selection regimes leading to evolutionary branching readily arise from a wide variety of different ecological interactions within and between species. We use classical ecological models for symmetric and asymmetric competition, for mutualism, and for predator‐prey interactions to describe evolving populations with continuously varying characters. For these models, we investigate the ecological and evolutionary conditions that allow for evolutionary branching and establish that branching is a generic and robust phenomenon. Evolutionary branching becomes a model for sympatric speciation when population genetics and mating mechanisms are incorporated into ecological models. In sexual populations with random mating, the continual production of intermediate phenotypes from two incipient branches prevents evolutionary branching. In contrast, when mating is assortative for the ecological characters under study, evolutionary branching is possible in sexual populations and can lead to speciation. Therefore, we also study the evolution of assortative mating as a quantitative character. We show that evolution under branching conditions selects for assortativeness and thus allows sexual populations to escape from fitness minima. We conclude that evolutionary branching offers a general basis for understanding adaptive speciation and radiation under a wide range of different ecological conditions.

Self-destructive cooperation mediated by phenotypic noise

In many biological examples of cooperation, individuals that cooperate cannot benefit from the resulting public good. This is especially clear in cases of self-destructive cooperation, where individuals die when helping others. If self-destructive cooperation is genetically encoded, these genes can only be maintained if they are expressed by just a fraction of their carriers, whereas the other fraction benefits from the public good. One mechanism that can mediate this differentiation into two phenotypically different sub-populations is phenotypic noise. Here we show that noisy expression of self-destructive cooperation can evolve if individuals that have a higher probability for self-destruction have, on average, access to larger public goods. This situation, which we refer to as assortment, can arise if the environment is spatially structured. These results provide a new perspective on the significance of phenotypic noise in bacterial pathogenesis: it might promote the formation of cooperative sub-populations that die while preparing the ground for a successful infection. We show experimentally that this model captures essential features of Salmonella typhimurium pathogenesis. We conclude that noisily expressed self-destructive cooperative actions can evolve under conditions of assortment, that self-destructive cooperation is a plausible biological function of phenotypic noise, and that self-destructive cooperation mediated by phenotypic noise could be important in bacterial pathogenesis.

A simple and general explanation for the evolution of altruism

We present a simple framework that highlights the most fundamental requirement for the evolution of altruism: assortment between individuals carrying the cooperative genotype and the helping behaviours of others with which these individuals interact. We partition the fitness effects on individuals into those due to self and those due to the ‘interaction environment’, and show that it is the latter that is most fundamental to understanding the evolution of altruism. We illustrate that while kinship or genetic similarity among those interacting may generate a favourable structure of interaction environments, it is not a fundamental requirement for the evolution of altruism, and even suicidal aid can theoretically evolve without help ever being exchanged among genetically similar individuals. Using our simple framework, we also clarify a common confusion made in the literature between alternative fitness accounting methods (which may equally apply to the same biological circumstances) and unique causal mechanisms for creating the assortment necessary for altruism to be favoured by natural selection.

Variable investment, the Continuous Prisoner's Dilemma, and the origin of cooperation

Cooperation is fundamental to many biological systems. A common metaphor for studying the evolution of cooperation is the Prisoners Dilemma, a game with two strategies: cooperate or defect. However, cooperation is rarely all or nothing, and its evolution probably involves the gradual extension of initially modest degrees of assistance. The inability of the Prisoners Dilemma to capture this basic aspect limits its use for understanding the evolutionary origins of cooperation. Here we consider a framework for cooperation based on the concept of investment: an act which is costly, but which benefits other individuals, where the cost and benefit depend on the level of investment made. In the resulting Continuous Prisoners Dilemma the essential problem of cooperation remains: in the absence of any additional structure non–zero levels of investment cannot evolve. However, if investments are considered in a spatially structured context, selfish individuals who make arbitrarily low investments can be invaded by higher–investing mutants. This results in the mean level of investment evolving to significant levels, where it is maintained indefinitely. This approach provides a natural solution to the fundamental problem of how cooperation gradually increases from a non–cooperative state.

EXPERIMENTAL EVIDENCE FOR SYMPATRIC ECOLOGICAL DIVERSIFICATION DUE TO FREQUENCY-DEPENDENT COMPETITION IN ESCHERICHIA COLI

Abstract We investigate adaptive diversification in experimental Escherichia coli populations grown in serial batch cultures on a mixture of glucose and acetate. All 12 experimental lines were started from the same genetically uniform ancestral strain but became highly polymorphic for colony size after 1000 generations. Five populations were clearly dimorphic and thus serve as a model for an adaptive lineage split. We analyzed the ecological basis for this dimorphism by studying bacterial growth curves. All strains exhibit diauxie, that is, sequential growth on the two resources. Thus, they exhibit phenotypic plasticity, using mostly glucose when glucose is abundant, then switching to acetate when glucose concentration is low. However, the coexisting strains differ in their diauxie pattern, with one cluster in the dimorphic populations growing better in the glucose phase, and the other cluster having a much shorter lag when switching to the acetate phase. Using invasion experiments, we show that the dimorphism of these two ecological types is maintained by frequency‐dependent selection. Using a mathematical model for the adaptive dynamics of diauxie behavior, we show that evolutionary branching in diauxie behavior is a plausible theoretical scenario. Our results support the hypothesis that, in our experiments, adaptive diversification from a genetically uniform ancestor occurred due to frequency‐dependent ecological interactions. Our results have implications for understanding the evolution of cross‐feeding polymorphism in microorganisms, as well as adaptive speciation due to frequency‐dependent selection on phenotypic plasticity.

A quantitative genetic competition model for sympatric speciation

I use multilocus genetics to describe assortative mating in a competition model. The intensity of competition between individuals is influenced by a quantitative character whose value is determined additively by alleles from many loci. With assortative mating based on this character, frequency‐ and density‐dependent competition can subdivide a population with an initially unimodal character distribution. The character distribution becomes bimodal, and the subpopulations corresponding to the two modes are reproductively separated because mating is assortative. This happens if the resource distribution is unimodal, i.e. even if selection due to phenotypic carrying capacities is not disruptive. The results suggest that sympatric speciation due to frequency‐dependent selection can occur in quite general ecological scenarios if mating is assortative. I also discuss the evolution of assortative mating. Since it induces bimodal phenotype distributions, assortative mating leads to a better match of the resources if their distribution is also bimodal. Moreover, in a population with a bimodal phenotype distribution, the average strength of frequency‐dependent competition is lower than in a unimodal population. Therefore, assortative mating permits higher equilibrium densities than random mating even if the resource distribution is unimodal. Thus, even though it may lead to a less efficient resource use, assortative mating is favoured over random mating because it reduces frequency‐dependent effects of competition.

Evolution of dispersal rates in metapopulation models : branching and cyclic dynamics in phenotype space

We study the evolution of dispersal rates in a two patch metapopulation model. The local dynamics in each patch are given by difference equations, which, together with the rate of dispersal between the patches, determine the ecological dynamics of the metapopulation. We assume that phenotypes are given by their dispersal rate. The evolutionary dynamics in phenotype space are determined by invasion exponents, which describe whether a mutant can invade a given resident population. If the resident metapopulation is at a stable equilibrium, then selection on dispersal rates is neutral if the population sizes in the two patches are the same, while selection drives dispersal rates to zero if the local abundances are different. With non‐equilibrium metapopulation dynamics, non‐zero dispersal rates can be maintained by selection. In this case, and if the patches are ecologically identical, dispersal rates always evolve to values which induce synchronized metapopulation dynamics. If the patches are ecologically different, evolutionary branching into two coexisting dispersal phenotypes can be observed. Such branching can happen repeatedly, leading to polymorphisms with more than two phenotypes. If there is a cost to dispersal, evolutionary cycling in phenotype space can occur due to the dependence of selection pressures on the ecological attractor of the resident population, or because phenotypic branching alternates with the extinction of one of the branches. Our results extend those of Holt and McPeek (1996), and suggest that phenotypic branching is an important evolutionary process. This process may be relevant for sympatric speciation.