Derek A. Roff

Natural selection and the heritability of fitness components.

The hypothesis that traits closely associated with fitness will generally possess lower heritabilities than traits more loosely connected with fitness is tested using 1120 narrow sense heritability estimates for wild, outbred animal populations, collected from the published record. Our results indicate that life history traits generally possess lower heritabilities than morphological traits, and that the means, medians, and cumulative frequency distributions of behavioural and physiological traits are intermediate between life history and morphological traits. These findings are consistent with popular interpretations of Fishers (1930, 1958) Fundamental Theorem of Natural Selection, and Falconer (1960, 1981), but also indicate that high heritabilities are maintained within natural populations even for traits believed to be under strong selection. It is also found that the heritability of morphological traits is significantly lower for ectotherms than it is for endotherms which may in part be a result of the strong correlation between life history and body size for many ectotherms.

Inbreeding depression in the wild

Despite its practical application in conservation biology and evolutionary theory, the cost of inbreeding in natural populations of plants and animals remains to a large degree unknown. In this review we have gathered estimates of inbreeding depression (δ) from the literature for wild species monitored in the field. We have also corrected estimates of δ by dividing by F (coefficient of inbreeding), to take into account the influence that the variation in F will have on δ. Our data set includes seven bird species, nine mammal species, four species of poikilotherms (snakes, fish and snails) and 15 plant species. In total we obtained 169 estimates of inbreeding depression for 137 traits; 81 of those estimates included estimates of F. We compared our mammalian data (limited to those traits related to juvenile mortality) to the estimates for captive zoo species published by Ralls et al. (1988) to determine if, as predicted from the literature, natural estimates of inbreeding depression are higher than captive estimates. The mean δ ± SE (significantly different from zero and not corrected for F) for homeotherms was 0.509 ± 0.081; for poikilotherms, 0.201 ± 0.039; and for plants, 0.331 ± 0.038. Levels of inbreeding depression this high in magnitude will be biologically important under natural conditions. When we limited our data set to mortality traits for mammals and corrected for F=0.25 (as is the case for the Ralls et al. data set), we found a significant difference between the two data sets; wild estimates had a substantially higher mean cost of inbreeding at F = 0.25: 2.155 (captive species: 0.314). Of the 169 estimates of δ, 90 were significantly different from zero, indicating that inbred wild species measured under natural conditions frequently exhibit moderate to high levels of inbreeding depression in fitness traits.

THE EVOLUTION OF WING DIMORPHISM IN INSECTS

Wing‐dimorphic insects are excellent subjects for a study of the evolution of dispersal since the nondispersing brachypterous morph is easily recognized. The purpose of this paper is to develop a framework within which the evolution of wing dimorphism can be understood. A review of the literature indicates that the presence or absence of wings may be controlled by a single locus, two‐allele genetic system or a polygenic system. Both types of inheritance can be subsumed within a general threshold model.

Quantitative genetics and fitness: lessons from Drosophila

This paper examines patterns of heritability and genetic covariance between traits in the genus Drosophila. Traits are divided into the categories, morphology, behaviour, physiology and life history. Early theoretical analyses suggested that life history traits should have heritabilities that are lower than those in other categories. Variable pleiotrophy, environmental variation, mutation and niche variation may, however, maintain high heritabilities. In Drosophila the heritabilities of life history traits are lower than morphological or physiological traits but may exceed 20 per cent. The pattern of variation in the heritability of behavioural traits is similar to that of life history traits. Genetic covariance between morphological traits and between morphological and life history traits are all positive but those between life history traits have variable sign. Negative covariance between traits supports the variable pleiotropy hypothesis but other factors such as environmental heterogeneity, or mutation cannot be excluded.

The evolution of trade-offs: where are we?

Trade‐offs are a core component of many evolutionary models, particularly those dealing with the evolution of life histories. In the present paper, we identify four topics of key importance for studies of the evolutionary biology of trade‐offs. First, we consider the underlying concept of ‘constraint’. We conclude that this term is typically used too vaguely and suggest that ‘constraint’ in the sense of a bias should be clearly distinguished from ‘constraint’ in the sense of proscribed combinations of traits or evolutionary trajectories. Secondly, we address the utility of the acquisition–allocation model (the ‘Y‐model’). We find that, whereas this model and its derivatives have provided new insights, a misunderstanding of the pivotal equation has led to incorrect predictions and faulty tests. Thirdly, we ask how trade‐offs are expected to evolve under directional selection. A quantitative genetic model predicts that, under weak or short‐term selection, the intercept will change but the slope will remain constant. Two empirical tests support this prediction but these are based on comparisons of geographic populations: more direct tests will come from artificial selection experiments. Finally, we discuss what maintains variation in trade‐offs noting that at present little attention has been given to this question. We distinguish between phenotypic and genetic variation and suggest that the latter is most in need of explanation. We suggest that four factors deserving investigation are mutation‐selection balance, antagonistic pleiotropy, correlational selection and spatio‐temporal variation, but as in the other areas of research on trade‐offs, empirical generalizations are impeded by lack of data. Although this lack is discouraging, we suggest that it provides a rich ground for further study and the integration of many disciplines, including the emerging field of genomics.

On Being the Right Size

Most examinations of body size center on a single factor. However, because body size is directly or indirectly linked to many, if not most, life history characters a more holistic approach is advocated. In this paper I present such an approach in the analysis of the optimum body size of Drosophila melanogaster. The basic life history parameters determining r are shown to be related to body size. Using these functions the relationship between r and body size is obtained. It is found that r is maximized within the observed range in size. A sensitivity analysis indicates that this result does not depend critically upon parameter estimation. This analysis also indicates that variation in egg size between geographic strains should be positively correlated to variation in body size. This prediction is shown to be correct. Reasonable variation in parameter values can account for much of the size range observed in the genus Drosophila. It does not appear to be possible to account for the very large size of certain Hawaiian species.

Optimizing development time in a seasonal environment: The ‘ups and downs’ of clinal variation

SummaryThis paper explores the problem of adapting development time to changes in the length of time conditions are favourable for growth and reproduction (‘season length’). It is shown that systematic changes in season length along some gradient such as latitude can generate either simple clines in development time or ‘saw-tooth’ clines. The relationship between development time and body size gives rise to a corresponding variation in body size. The generation of a ‘saw-tooth’ cline does not require sharp environmental changes. Both types of clinal variation are observed in insects.

Effect of extrinsic mortality on the evolution of senescence in guppies.

Classical theories for the evolution of senescence predict that organisms that experience low mortality rates attributable to external factors, such as disease or predation, will evolve a later onset of senescence. Here we use patterns of senescence in guppies derived from natural populations that differ in mortality risk to evaluate the generality of these predictions. We have previously found that populations experiencing higher mortality rates evolve earlier maturity and invest more in reproduction, as predicted by evolutionary theory. We report here that these same populations do not have an earlier onset of senescence with respect to either mortality or reproduction but do with respect to swimming performance, which assesses neuromuscular function. This mosaic pattern of senescence challenges the generality of the association between decreased extrinsic mortality and delayed senescence and invites consideration of more derived theories for the evolution of senescence.

THE EVOLUTION OF GENETIC CORRELATIONS : AN ANALYSIS OF PATTERNS

The genetic correlation is a central parameter of quantitative genetics, providing a measure of the rate at which traits respond to indirect selection (i.e., selection that does not act upon the traits under study, but some other trait with which they have genes in common). In this paper, I review the pattern of variation among four combinations of traits: life history × life history (L × L), morphological × morphological (M × M), life history × morphological (L × M), and behavioral × behavioral (B × B). A few other combinations were investigated, but insufficient data were obtained for separate analysis. A total of 1798 correlations, distributed over 51 different animal and plant species, were analyzed. The analysis was conducted at two levels: first by dividing the data set solely by trait combination, and second by blocking the data by trait combination and species. Because selection will tend to fix alleles that show positive correlations with fitness traits faster than those that are negative and because the latter are expected to arise more frequently by mutation, correlations between life‐history traits are predicted to be more often negative than those between morphological traits. This prediction was supported, with the ranking in decreasing proportion of negative correlations being: L × L > L × M > B × B > M × M. The mean magnitude of the genetic correlation shows little variation among morphological and life‐history combinations, and the distribution of values is remarkably flat. However, the estimated standard errors and the coefficient of variation (SE/rG) are large, making it difficult to separate biological factors influencing the pattern of dispersion from experimental error. Analysis of the phenotypic and genetic correlations suggest that for the combinations M × M and L × M, but not L × L or B × B, the phenotypic correlation is an adequate estimate of the genetic correlation.

A comparison of inbreeding depression in life-history and morphological traits in animals

The current study tests the hypothesis that life‐history traits (closely related to fitness) show greater inbreeding depression than morphological traits (less closely related to fitness). The mean and median slope of the standardized coefficient of inbreeding depression (the slope of the linear relationship between F and the trait value) for life‐history and morphological traits were compared. Slopes for life‐history traits were higher than those for morphological traits. At F = 0.25 (full‐sibling mating), life‐history traits experienced a median reduction of 11.8% in trait value, whereas morphological traits showed a depression in trait value of approximately 2.2%.