H. Allen Orr

Patterns of speciation in Drosophila

To investigate the time course of speciation, we gathered literature data on 119 pairs of closely related Drosophila species with known genetic distances, mating discrimination, strength of hybrid sterility and inviability, and geographic ranges. Because genetic distance is correlated with divergence time, these data provide a cross‐section of taxa at different stages of speciation.

The genetic theory of adaptation: a brief history

Theoretical studies of adaptation have exploded over the past decade. This work has been inspired by recent, surprising findings in the experimental study of adaptation. For example, morphological evolution sometimes involves a modest number of genetic changes, with some individual changes having a large effect on the phenotype or fitness. Here I survey the history of adaptation theory, focusing on the rise and fall of various views over the past century and the reasons for the slow development of a mature theory of adaptation. I also discuss the challenges that face contemporary theories of adaptation.

THE POPULATION GENETICS OF ADAPTATION : THE DISTRIBUTION OF FACTORS FIXED DURING ADAPTIVE EVOLUTION

We know very little about the genetic basis of adaptation. Indeed, we can make no theoretical predictions, however heuristic, about the distribution of phenotypic effects among factors fixed during adaptation nor about the expected “size” of the largest factor fixed. Study of this problem requires taking into account that populations gradually approach a phenotypic optimum during adaptation via the stepwise substitution of favorable mutations. Using Fishers geometric model of adaptation, I analyze this approach to the optimum, and derive an approximate solution to the size distribution of factors fixed during adaptation. I further generalize these results to allow the input of any distribution of mutational effects. The distribution of factors fixed during adaptation assumes a pleasingly simple, exponential form. This result is remarkably insensitive to changes in the fitness function and in the distribution of mutational effects. An exponential trend among factors fixed appears to be a general property of adaptation toward a fixed optimum.

THE EVOLUTION OF POSTZYGOTIC ISOLATION: ACCUMULATING DOBZHANSKY-MULLER INCOMPATIBILITIES

Abstract.— Hybrid sterility and inviability often result from the accumulation of substitutions that, while functional on their normal genetic backgrounds, cause a loss of fitness when brought together in hybrids. Previous theory has shown that such Dobzhansky‐Muller incompatibilities should accumulate at least as fast as the square of the number of substitutions separating two species, the so‐called snowball effect. Here we explicitly describe the stochastic accumulation of these incompatibilities as a function of time. The accumulation of these incompatibilities involves three levels of stochasticity: (1) the number of substitutions separating two allopatric lineages at a given time; (2) the number of incompatibilities resulting from these substitutions; and (3) the fitness effects of individual incompatibilities. Previous analyses ignored the stochasticity of molecular evolution (level 1) as well as that due to the variable effects of incompatibilities (level 3). Here we approximate the full stochastic process characterizing the accumulation of hybrid incompatibilities between pairs of loci. We derive the distribution of the number of incompatibilities as a function of divergence time between allopatric taxa as well as the distribution of waiting times to speciation by postzygotic isolation. We provide simple approximations for the mean and variance of these waiting times. These results let us estimate, albeit crudely, the probability, p, that two diverged sites from different species will contribute to hybrid sterility or inviability. Our analyses of data from Drosophila and Bombina suggest that p is generally very small, on the order of 10−6 or less.

Adaptation and the cost of complexity.

Abstract.— Adaptation is characterized by the movement of a population toward a many‐character optimum, movement that results in an increase in fitness. Here I calculate the rate at which fitness increases during adaptation and describe the curve giving fitness versus time as a population approaches an optimum in Fishers model of adaptation. The results identify several factors affecting the speed of adaptation. One of the most important is organismal complexity—complex organisms adapt more slowly than simple ones when using mutations of the same phenotypic size. Thus, as Fisher foresaw, organisms pay a kind of cost of complexity. However, the magnitude of this cost is considerably larger than Fishers analysis suggested. Indeed the rate of adaptation declines at least as fast as n‐1, where n is the number of independent characters or dimensions comprising an organism. The present results also suggest that one can define an effective number of dimensions characterizing an adapting species.

A Single Gene Causes Both Male Sterility and Segregation Distortion in Drosophila Hybrids

A central goal of evolutionary biology is to identify the genes and evolutionary forces that cause speciation, the emergence of reproductive isolation between populations. Despite the identification of several genes that cause hybrid sterility or inviability—many of which have evolved rapidly under positive Darwinian selection—little is known about the ecological or genomic forces that drive the evolution of postzygotic isolation. Here, we show that the same gene, Overdrive, causes both male sterility and segregation distortion in F1 hybrids between the Bogota and U.S. subspecies of Drosophila pseudoobscura. This segregation distorter gene is essential for hybrid sterility, a strong reproductive barrier between these young taxa. Our results suggest that genetic conflict may be an important evolutionary force in speciation.

THE POPULATION GENETICS OF ADAPTATION: THE ADAPTATION OF DNA SEQUENCES

Abstract I describe several patterns characterizing the genetics of adaptation at the DNA level. Following Gillespie (1983, 1984, 1991), I consider a population presently fixed for the ith best allele at a locus and study the sequential substitution of favorable mutations that results in fixation of the fittest DNA sequence locally available. Given a wild type sequence that is less than optimal, I derive the fitness rank of the next allele typically fixed by natural selection as well as the mean and variance of the jump in fitness that results when natural selection drives a substitution. Looking over the whole series of substitutions required to reach the best allele, I show that the mean fitness jumps occurring throughout an adaptive walk are constrained to a twofold window of values, assuming only that adaptation begins from a reasonably fit allele. I also show that the first substitution and the substitution of largest effect account for a large share of the total fitness increase during adaptation. I further show that the distribution of selection coefficients fixed throughout such an adaptive walk is exponential (ignoring mutations of small effect), a finding reminiscent of that seen in Fishers geometric model of adaptation. Last, I show that adaptation by natural selection behaves in several respects as the average of two idealized forms of adaptation, perfect and random.

Speciation by postzygotic isolation: forces, genes and molecules

New species arise as reproductive isolation evolves between diverging populations. Here we review recent work in the genetics of postzygotic reproductive isolation—the sterility and inviability of species hybrids. Over the last few years, research has taken two new directions. First, we have begun to learn a good deal about the population genetic forces driving the evolution of postzygotic isolation. It has, for instance, become increasingly clear that conflict‐driven processes, like sexual selection and meiotic drive, may contribute to the evolution of hybrid sterility. Second, we have begun to learn something about the identity and molecular characteristics of the actual genes causing hybrid problems. Although molecular genetic data are limited, early findings suggest that “speciation genes” correspond to loci having normal functions within species and that these loci sometimes diverge as a consequence of evolution in gene regulation. BioEssays 22:1085–1094, 2000.

Gene transposition as a cause of hybrid sterility in Drosophila.

We describe reproductive isolation caused by a gene transposition. In certain Drosophila melanogaster–D. simulans hybrids, hybrid male sterility is caused by the lack of a single-copy gene essential for male fertility, JYAlpha. This gene is located on the fourth chromosome of D. melanogaster but on the third chromosome of D. simulans. Genomic and molecular analyses show that JYAlpha transposed to the third chromosome during the evolutionary history of the D. simulans lineage. Because of this transposition, a fraction of hybrids completely lack JYAlpha and are sterile, representing reproductive isolation without sequence evolution.

Population Extinction and the Genetics of Adaptation

Theories of adaptation typically ignore the effect of environmental change on population size. But some environmental challenges—challenges to which populations must adapt—may depress absolute fitness below 1, causing populations to decline. Under this scenario, adaptation is a race; beneficial alleles that adapt a population to the new environment must sweep to high frequency before the population becomes extinct. We derive simple, though approximate, solutions to the probability of successful adaptation (population survival) when adaptation involves new mutations, the standing genetic variation, or a mixture of the two. Our results show that adaptation to such environmental challenges can be difficult when relying on new mutations at one or a few loci, and populations will often decline to extinction.