Joel R. Peck

Recent advances in understanding of the evolution and maintenance of sex

The evolution of sex has been the focus of considerable attention during recent years. There is some consensus that the solution to the mystery is that sex either enables the creation and spread of advantageous traits (possibly parasite resistance) or helps to purge the genome of deleterious mutations. Recent experimental work has allowed testing of some of the assumptions underlying the theoretical models, most particularly whether interactions between genes are synergistic and whether the mutation rate is adequately high. However, although a variety of theories point out advantages to sex, most of them predict that a little sex and recombination can go a long way towards improving the fitness of a population, and it remains unclear why obligate sex is so common.

Explaining the geographic distributions of sexual and asexual populations

Examination of the geographic distributions of sexual organisms and their asexual, or parthenogenetic, competitors reveals certain consistent patterns. These patterns are called geographic parthenogenes is. For example, if we compare sexual organisms with closely related asexuals, we find that, in the Northern Hemisphere, there is a strong tendency for the asexuals to occur further to the north. One researcher to document this pattern is Bierzychudek, who examined 43 cases (drawn from 10 genera) where the geographic distributions of a sexual plant and a closely related asexual are known. In 76% of these cases, the asexual plants range was more northerly than the range of the sexual. Some of the remaining cases probably fit with this pattern, but more data must be obtained before this suggestion can be confirmed. Asexuals also tend to occur at high altitudes, and in marginal, resource-poor environments. We have constructed a mathematical model of a habitat that stretches from south to north in the Northern Hemisphere. Our computer simulations based on this model support the idea that a single basic process may account for much of what is known about geographic parthenogenesis. This process involves the movement of individuals from areas in which they are well adapted to areas where they are poorly adapted.

Pleiotropic scaling of gene effects and the 'cost of complexity'.

As perceived by Darwin, evolutionary adaptation by the processes of mutation and selection is difficult to understand for complex features that are the product of numerous traits acting in concert, for example the eye or the apparatus of flight. Typically, mutations simultaneously affect multiple phenotypic characters. This phenomenon is known as pleiotropy. The impact of pleiotropy on evolution has for decades been the subject of formal analysis. Some authors have suggested that pleiotropy can impede evolutionary progress (a so-called ‘cost of complexity’). The plausibility of various phenomena attributed to pleiotropy depends on how many traits are affected by each mutation and on our understanding of the correlation between the number of traits affected by each gene substitution and the size of mutational effects on individual traits. Here we show, by studying pleiotropy in mice with the use of quantitative trait loci (QTLs) affecting skeletal characters, that most QTLs affect a relatively small subset of traits and that a substitution at a QTL has an effect on each trait that increases with the total number of traits affected. This suggests that evolution of higher organisms does not suffer a ‘cost of complexity’ because most mutations affect few traits and the size of the effects does not decrease with pleiotropy.

The Evolution of Helping Behavior in Large, Randomly Mixed Populations

A model is presented in which individuals who perform helping behavior can increase in frequency from low initial levels in a large population within which interactions take place between randomly selected individuals. This is accomplished without requiring extreme conditions. The model uses a payoff matrix that determines the consequences of each possible type of interaction between individuals. This payoff matrix changes as a function of the genetic constitution of the population. As a result, the payoff matrix may or may not satisfy the inequalities that define the prisoners dilemma, a formal game commonly used to study the evolution of helping behavior. An analysis of the model reveals that, for a wide range of parameter values, all stable equilibria occur at points where the genetic constitution of the population allows for satisfaction of the prisoners-dilemma inequalities. This is the case even though these inequalities may not be satisfied during the initial stages of invasions by helpers.

The evolution of outsider exclusion

The rate of migration between different parts of a population can be important in determining evolutionary outcomes. This paper presents a mathematical model in which some individuals act to exclude immigrants from their group. It is shown that outsider exclusion can be favoured by evolution, even when outsider excluders incur a large cost. In addition, it is shown that the evolutionary mechanism which causes increases in the frequency of outsider excluders is a form of kin selection or group selection. A second model shows that a similar mechanisms can act to favour the evolution of reluctance to mate with immigrants.

Mutation and sex in a competitive world

How do deleterious mutations interact to affect fitness? The answer to this question has substantial implications for a variety of important problems in population biology, including the evolution of sex, the rate of adaptation and the conservation of small populations. Here we analyse a mathematical model of competition for food in which deleterious mutations affect competitive ability. We show that, if individuals usually compete in small groups, then competition can easily lead to a type of genetic interaction known as synergistic epistasis. This means that a deleterious mutation is most damaging in a genome that already has many other deleterious mutations. We also show that competition in small groups can produce a large advantage for sexual populations, both in mean fitness and in ability to resist invasion by asexual lineages. One implication of our findings is that experimental efforts to demonstrate synergistic epistasis may not succeed unless the experiments are redesigned to make them much more naturalistic.

Group selection, individual selection, and the evolution of genetic drift*

In a subdivided population, genetic drift affects variation between groups, and thus it can have an important effect on the outcome of evolution (Wright, 1978). The rate of genetic drift is determined, in part, by the behaviour of population members. This paper presents three mathematical models in which behavioural traits that affect the rate of genetic drift are allowed to coevolve with traits that are under selection at the group and individual levels. The results show that if group selection is strong relative to individual selection, then behavioural traits that enhance the rate of genetic drift will tend to increase in frequency. The strength of this effect depends, in part, on the way in which vacant sites are colonized.

What's wrong with a little sex?

In many species, most (or all) offspring are produced by sexual means. However, theory suggests that selection should often favour the evolution of species in which a small fraction of offspring are produced sexually, and the rest are produced asexually. Here, we present the analysis of a model that may help to resolve this paradox. We show that, when heterozygote advantage is in force, members of species in which sex is rare will tend to produce poorly adapted offspring when they mate. This problem should be less severe in species where most offspring are produced by sexual means. As a consequence, once the rate of sexual reproduction becomes sufficiently rare, the benefits of sex may vanish, leading to the evolution of obligate asexuality. Substantial benefits of sexual reproduction may tend to accrue only if a large proportion of offspring are produced sexually. We suggest that similar findings are likely in the case of epistatic interactions between loci.

The maintenance of sexual reproduction in a structured population

We present the results of a computer simulation model in which a sexual population produces an asexual mutant. We estimate the probability that the new asexual lineage will go extinct. We find that whenever the asexual lineage does not go extinct the sexual population is out–competed, and only asexual individuals remain after a sufficiently long period of time has elapsed. We call this type of outcome an asexual takeover. Our results suggest that, given repeated mutations to asexuality, asexual takeover is likely in an unstructured environment. However, if the environment is subdivided into demes that are connected by migration, then asexual takeover becomes less likely. The probability of asexual takeover declines towards zero as the number of demes increases and as the rate of migration decreases. The reason for this is that asexuality leads to a greater loss of fitness due to mutation and genetic drift, in comparison to what occurs under sexual reproduction. Population subdivision slows the spread of asexual lineages, which allows more time for the genetic degeneration caused by asexuality to take place.

Frequency-dependent selection, beneficial mutations, and the evolution of sex

This paper presents a mathematical model of a population in which multiple alleles at a particular locus are maintained by frequency-dependent selection. The results suggest that, if the population reproduces sexually, the benefit conferred on the population by beneficial mutations at other loci will typically be much larger than if the population reproduces by asexual means. In part, this is true because, in asexual populations, beneficial mutations can produce suboptimal distributions of the alleles that are subject to frequency-dependent selection. Another factor that produces an advantage for sex is that, in asexual populations, beneficial mutations that have achieved a high copy number may nevertheless be lost from the population. This is highly unlikely in sexual populations.