Trevor D. Price

The role of phenotypic plasticity in driving genetic evolution.

Models of population divergence and speciation are often based on the assumption that differences between populations are due to genetic factors, and that phenotypic change is due to natural selection. It is equally plausible that some of the differences among populations are due to phenotypic plasticity. We use the metaphor of the adaptive landscape to review the role of phenotypic plasticity in driving genetic evolution. Moderate levels of phenotypic plasticity are optimal in permitting population survival in a new environment and in bringing populations into the realm of attraction of an adaptive peak. High levels of plasticity may increase the probability of population persistence but reduce the likelihood of genetic change, because the plastic response itself places the population close to a peak. Moderate levels of plasticity arise whenever multiple traits, some of which are plastic and others not, form a composite trait involved in the adaptive response. For example, altered behaviours may drive selection on morphology and physiology. Because there is likely to be a considerable element of chance in which behaviours become established, behavioural change followed by morphological and physiological evolution may be a potent force in driving evolution in novel directions. We assess the role of phenotypic plasticity in stimulating evolution by considering two examples from birds: (i) the evolution of red and yellow plumage coloration due to carotenoid consumption; and (ii) the evolution of foraging behaviours on islands. Phenotypic plasticity is widespread in nature and may speed up, slow down, or have little effect on evolutionary change. Moderate levels of plasticity may often facilitate genetic evolution but careful analyses of individual cases are needed to ascertain whether plasticity has been essential or merely incidental to population differentiation.

LIKELIHOOD OF ANCESTOR STATES IN ADAPTIVE RADIATION

Theories of ecological diversification make predictions about the timing and ordering of character state changes through history. These theories are testable by “reconstructing” ancestor states using phylogenetic trees and measurements of contemporary species. Here we use maximum likelihood to estimate and evaluate the accuracy of ancestor reconstructions. We present likelihoods of discrete ancestor states and derive probability distributions for continuous ancestral traits. The methods are applied to several examples: diets of ancestral Darwins finches; origin of inquilinism in gall wasps; microhabitat partitioning and body size evolution in scrubwrens; digestive enzyme evolution in artiodactyl mammals; origin of a sexually selected male trait, the sword, in platies and swordtails; and evolution of specialization in Anolis lizards. When changes between discrete character states are rare, the maximum‐likelihood results are similar to parsimony estimates. In this case the accuracy of estimates is often high, with the exception of some nodes deep in the tree. If change is frequent then reconstructions are highly uncertain, especially of distant ancestors. Ancestor states for continuous traits are typically highly uncertain. We conclude that measures of uncertainty are useful and should always be provided, despite simplistic assumptions about the probabilistic models that underlie them. If uncertainty is too high, reconstruction should be abandoned in favor of approaches that fit different models of trait evolution to species data and phylogenetic trees, taking into account the range of ancestor states permitted by the data.

THE EVOLUTION OF F1 POSTZYGOTIC INCOMPATIBILITIES IN BIRDS

Abstract We analyzed the rate at which postzygotic incompatibilities accumulate in birds. Our purposes were to assess the role of intrinsic F1 hybrid infertility and inviability in the speciation process, and to compare rates of loss of fertility and viability between the sexes. Among our sample more than half the crosses between species in the same genus produce fertile hybrids. Complete loss of F1 hybrid fertility takes on the order of millions of years. Loss of F1 hybrid viability occurs over longer timescales than fertility: some viable hybrids have been produced between taxa that appear to have been separated for more than 55 my. There is strong support for Haldanes rule, with very few examples where the male has lower fitness than the female. However, in contrast to Drosophila, fertility of the homogametic sex in the F1 appears to be lost before viability of the heterogametic sex in the F1. We conclude that the time span of loss of intrinsic hybrid fertility and viability is often, but not always, longer than the time to speciation. Premating isolation is an important mechanism maintaining reproductive isolation in birds. In addition, other factors causing postzygotic reproductive isolation such as ecological causes of hybrid unfitness, reduced mating success of hybrids, and genetic incompatibilities in the F2s and backcrosses may often be involved in the speciation process.

ON THE LOW HERITABILITY OF LIFE-HISTORY TRAITS

Life‐history traits such as longevity and fecundity often show low heritability. This is usually interpreted in terms of Fishers fundamental theorem to mean that populations are near evolutionary equilibrium and genetic variance in total fitness is low. We develop the causal relationship between metric traits and life‐history traits to show that a life‐history trait is expected to have a low heritability whether or not the population is at equilibrium. This is because it is subject to all the environmental variation in the metric traits that affect it plus additional environmental variation. There is no simple prediction regarding levels of additive genetic variance in life‐history traits, which may be high at equilibrium. Several other patterns in the inheritance of life‐history traits are readily predicted from the causal model. These include the strength of genetic correlations between life‐history traits, levels of nonadditive genetic variance, and the inevitability of genotype‐environment interaction.

SPECIATION BY REINFORCEMENT OF PREMATING ISOLATION

The generation of premating isolation given partial or complete postzygotic isolation between populations is termed reinforcement or, in the case of complete isolation, reproductive character displacement. In this study we use computer simulations and a multilocus genetic model to reevaluate the theory of reinforcement. We consider the evolution of female preferences for a male secondary sexual trait. If the populations differ in mean female preference, there is direct selection on the preference for further divergence, which may be augmented by a correlated response to sexual selection on males. Two factors prevent divergence. First, if postzygotic isolation is not complete, gene flow can prevent divergence and lead to a hybrid swarm. This is the usual outcome whenever the average number of breeding adult offspring produced by a hybrid mating is sufficient to replace the parents. Second, one or the other population may become extinct because of the large number of hybrid matings it is involved in. The likelihood of extinction is lowered if population growth rates are high, if hybrids are inviable rather than infertile, or under some conditions when allopatric populations provide immigrants into the contact zone. Provided hybrid fitness is sufficiently low, there is a wide range of genetic and ecological conditions under which reinforcement rather easily occurs, and also a range under which it may occur because of stochastic effects on both the inheritance parameters and the population sizes.

Density-Dependent Cladogenesis in Birds

A characteristic signature of adaptive radiation is a slowing of the rate of speciation toward the present. On the basis of molecular phylogenies, studies of single clades have frequently found evidence for a slowdown in diversification rate and have interpreted this as evidence for density dependent speciation. However, we demonstrated via simulation that large clades are expected to show stronger slowdowns than small clades, even if the probability of speciation and extinction remains constant through time. This is a consequence of exponential growth: clades, which, by chance, diversify at above the average rate early in their history, will tend to be large. They will also tend to regress back to the average diversification rate later on, and therefore show a slowdown. We conducted a meta-analysis of the distribution of speciation events through time, focusing on sequence-based phylogenies for 45 clades of birds. Thirteen of the 23 clades (57%) that include more than 20 species show significant slowdowns. The high frequency of slowdowns observed in large clades is even more extreme than expected under a purely stochastic constant-rate model, but is consistent with the adaptive radiation model. Taken together, our data strongly support a model of density-dependent speciation in birds, whereby speciation slows as ecological opportunities and geographical space place limits on clade growth.

Honesty, perception and population divergence in sexually selected traits.

We investigate the evolution of female preference for one and two male ornaments, to address two issues in sexual selection: (i) what factors affect the evolution of female preferences; and (ii) how do preferences diverge between isolated populations, leading to speciation? We assume that the male traits are costly indicators of male condition (‘handicaps’), and that females benefit directly from a high-condition mate. We find that optimal female preference for a single male trait equals (benefit of condition) x (detectability of male trait) x (honesty of male trait) / (costliness of preference). With two male traits to choose from, females should prefer the one with greatest honesty x detectability, and ignore the second. These results highlight the role of perception in the evolution of both male ornaments and female preferences, and provide a theoretical illustration of ‘sensory drive’. They confirm that a less honest male trait can displace a more honest trait if its detectability is sufficiently high. Environmental differences can drive evolutionary divergence between populations in both the male trait and female preference. Even small differences between habitats in detectability of male traits can trigger dramatic change in the female preference. Finally, populations may drift apart in arbitrary directions if choice of different male traits yields equivalent benefits to females.

Adaptive Phenotypic Plasticity and the Successful Colonization of a Novel Environment

Behavior and other forms of phenotypic plasticity potentially enable individuals to deal with novel situations. This implies that establishment of a population in a new environment is aided by plastic responses, as first suggested by Baldwin (1896). In the early 1980s, a small population of dark‐eyed juncos from a temperate, montane environment became established in a Mediterranean climate in coastal San Diego. The breeding season of coastal juncos is more than twice as long as that of the ancestral population, and they fledge approximately twice as many young. We investigated the adaptive significance of the longer breeding season and its consequences for population persistence. Within the coastal population, individuals with longer breeding seasons have higher offspring production and recruitment, with no measured detrimental effects such as higher mortality or lower reproductive success the following year. Population size has remained approximately constant during the 6 years of study (1998–2003). The increase in reproductive effort in the coastal population contributes substantially to the persistence of this population because there is no evidence of density‐dependent recruitment, which would otherwise negate the effects of increased fledgling production. These results provide the first quantitative support of Baldwin’s proposition that plasticity can be crucial for population persistence during the early stages of colonization.

Conflicting Selection Pressures and Life History Trade-Offs

We review studies of natural selection in wild populations in which selection has acted in opposite directions at different stages of the life history. For example, the phenotype with highest probability of survival may have the lowest reproductive success. We discuss two important implications of these findings. First, measurements of opposing selection confirm that evolution of traits is governed by a balance of conflicting fitness advantages. Second, studies of opposing selection are informative about mechanisms underlying life history trade-offs. We outline difficulties in measuring opposing selection, particularly the problem that patterns of selection may be masked by the positive effects of nutrition on size of metric traits and fitness components. We discuss some solutions to these problems, and present a statistical technique to help disentangle direct selection from nutritional effects. Finally, we show how fluctuations in selection pressures lead to norms of reaction for life history traits in the absence of developmental plasticity.

Sexual imprinting, learning and speciation

Learned mate preferences may play an important role in speciation. Sexual imprinting is a process whereby mate preferences are affected by learning at a very young age, usually using a parent as the model. We suggest that while the origins of learning appear to lie in the advantages of individual recognition, sexual imprinting results from selection for recognition of conspecifics. This is because efficient early learning about one’s own species is favoured in the presence of heterospecifics. If different species are hybridizing, both sexual imprinting and learning to avoid heterospecifics during adulthood promote assortative mating and hence speciation. As a result of sexual imprinting, speciation may also be completed in allopatry when divergence between populations is sufficient to prevent interbreeding when the populations reunite, even in the absence of genetic evolution of mate preference. The role of behaviour and learning in completing the speciation process is relatively overlooked. In particular the evolution of sexual imprinting as a result of selection against hybridization warrants more study.