Edwin H. Bryant
State University of New York System
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Evolution | 1977
Edwin H. Bryant
It has long been recognized that morphometric difference among geographic populations of a species can reveal modes of adaptation to environment and of eventual speciation. Most early studies of such variation were limited to few characters (e.g., Alpatov, 1929; Dobzhansky, 1933), and not until the advent of computers could large suites of characters be analyzed by appropriate techniques of covariation, such as principal component or factor analysis, to isolate and identify underlying patterns of morphogenesis (Blackith, 1960). The statistical revolution in geographic variation analysis, however, has not generated a similar revolution of insight into population dynamics, and for the most part, morphometric approaches have been abandoned by population biologists uninterested in systematics. A part of this problem is that few modern studies attempt to separate spatial from temporal aspects of variability or genetic causation from environmental induction of phenotype, typically present in early work (e.g., Goldschmidt, 1934; Stalker and Carson, 1947, 1948, 1949). This paper attempts to partition morphometric variation in the housefly, Musca domestica L., in the United States into temporal, spatial, and genetic components, and thereby elucidate the dynamics of adaptation to differing environments in this species. The lack of systematically recognized variatioi of the housefly in the United States offers reasonable assurance of common niche and habitat requirements of flies from widespread populations, so that sample partitions of variation can be compared to reveal trends of populational adaptation to changing environments. The essence of the methodology utilized here, paralleling an analysis of variance, was to collect flies from numerous localities throughout the United States, return to selected localities at the same times in subsequent years to assess year-to-year variation within sites, and then to follow at least one population throughout the year to determine a seasonal component of morphometric change. Thus variance components can be estimated at these various levels of potential variation, to discern underlying causes of morphometric adaptation. Comparisons among repeated collections within localities and between wild and laboratory reared flies were used to determine repeatability and consistency in patterns of covariation and to ascertain the extent of genetic commitment to morphometric response.
Heredity | 1993
Edwin H. Bryant; Lisa M. Meffert
Experimental populations of the housefly, initiated from a single outbred natural population, were subjected to five serial founder events of one, four, or 16 pairs of flies. After each bottleneck the populations were allowed to flush to approximately 1000 pairs, at which time they were assayed for additive genetic variance for eight morphometric traits using parental–offspring covariances. Additive genetic variance for all bottleneck sizes rose above the level of the outbred control in response to the first bottleneck and remained comparable to or higher than that of the control over most of the successive bottleneck episodes; no bottleneck size exhibited additive genetic variance significantly below the level of the control throughout the experiment. Such changes in additive genetic variance in response to bottlenecks are inconsistent with a model of neutral additive gene action, suggesting that non-additive components of genetic variance are likely to have affected the traits. Two models of non-additive genetic variance, pure dominance and additive-by-additive epistasis, provided reasonable fits to our data, but were not distinguishable from each other. Both empirical and theoretical results suggest that additive genetic variance for quantitative traits can remain high despite repeated reduction of the population size to as low as a single mated pair. Historical bottlenecks cannot be accurately inferred from levels of additive genetic variance for complex quantitative characters that are affected by non-additive components of genetic variance.
Evolution | 1991
Lisa M. Meffert; Edwin H. Bryant
The efficacy of bottlenecks to stimulate divergence in courtship behavior and consequent premating isolation was tested by serial founder‐flush episodes of three sizes (one, four, or 16 pairs) on a population of houseflies established in the laboratory from a single field population. After the fifth founder‐flush episode, intraline and interline crosses were performed to detect divergence in mating propensities and patterns of assortative mating. Videotapings of intraline courtships for the bottleneck lines and the control were evaluated for changes in courtship repertoire. All bottleneck lines showed significant divergence from the control in male and/or female mating propensity and in courtship behavior. Divergence from the control was bidirectional for both male and female mating propensities as well as for courtship element utilization. Out of 15 tests for assortative mating between bottleneck lines and between bottleneck lines and the control, only two cases of positive assortative mating and one case of negative assortative mating were detected. Because some bottleneck lines showed increased courtship element utilization and because decreased courtship utilization in some bottleneck lines was related to higher male mating success, the mechanisms behind the Kaneshiro model (which is based upon ancestral females discriminating against bottleneck males that had “lost” courtship elements) were not supported in general. A partitioning effect of the bottlenecks upon the intrinsic variation in the ancestral population for courtship pattern appeared to explain a large component of the directions of divergence from the control. Still, the pattern of divergence of some bottleneck lines apparently was not constrained by the intercorrelation structure of courtship behaviors detected in the control. Because previous studies showed that the bottleneck lines had rebounded from inbreeding depression to fitness levels of the control, this study documents nondebilitating differentiation in the courtship repertoire that can account for divergent mating propensities and premating isolation.
The American Naturalist | 1990
Edwin H. Bryant; Lisa M. Meffert; Steven A. McCommas
Critics of theories of speciation via bottlenecks have argued that the loss of genetic variation as a result of a bottleneck would be sufficient toretard adaptation in founder populations or, in terms of Wrights adaptive-topography model, would lower the chance of a peak shift in relation to an outbred population (B. Charlesworth and Smith 1982; Barton and Charlesworth 1984; B. Charlesworth and Rouhani 1988). However, we have shown that additive genetic variation can actually increase in experimentally bottlenecked lines of the house fly (Bryant et al. 1986). More specifically, when dominance and epistasis contribute to the genetic variance, a portion of this nonadditive variance can be converted into additive genetic variance during a bottleneck to increase the overall level of additive genetic variance available for selectional response (Robertson 1952; Goodnight 1987, 1988). As a result, additive genetic variation would become available to a founder population when selection may be most intense in the invasion of a new territory. The major problem of such a scenario is that several measures of fitness in our bottleneck lines declined in relationship to the control line (Bryant et al. 1986, fig. 3). If this lowered fitness were to persist, these lines would not be viable progenitors of future populations (Hedrick 1987). In making such an assessment, however, it is important to follow the fitness of bottleneck lines for a longer period. Not all individuals within an inbred population are necessarily inbred to the same degree (Avery and Hill 1977, 1979; Franklin 1977; Weir et al. 1980; Cockerham and Weir 1983), and if there is a correlation between degree of inbreeding and fitness within these populations, natural selection could quickly restore fitness. This note reports on the changing fitness of our bottleneck lines through five successive bottleneck cycles. Although inbreeding depression is well documented in many organisms, particularly for Drosophila and Mus (review in D. Charlesworth and Charlesworth 1987), few studies have followed fitness changes of individual ines (Dobzhansky and Spassky 1947; Hollingsworth and Maynard Smith 1955); thus, recovery from inbreeding depression in most cases has been due to differential survival among inbred lines and not due to changes within
Heredity | 1990
Steven A. McCommas; Edwin H. Bryant
Experimental bottleneck lines were generated from a single outbred population of the housefly using one, four, or 16 pairs of flies. These lines were followed through one, three, or five successive founder-flush cycles. After each flush 30 individuals from each line were assayed for electrophoretic variation at four initially polymorphic loci. Electrophoretic variation largely followed neutral expectation, the major exception being that the differentiation among 16-pair lines was greater than expected. All bottleneck sizes showed significant losses in genetic variation compared to the control, particularly for losses in numbers of alleles. These findings contrast theoretical predictions in that few lines and loci would be required to detect historical bottlenecks.
Evolution | 1988
Edwin H. Bryant; Lisa M. Meffert
Three measures of multivariate integration were derived from both additive genetic covariance and correlation matrices estimated from parent‐offspring covariances to investigate the effect of bottlenecks of different sizes on genetic integration of morphological traits in the housefly, Musca domestica L. Bottleneck lines were initiated with one, four, or 16 pairs of flies sampled from a natural outbred (control) population. Bottlenecks of intermediate size significantly increased the average genetic correlation among traits, resulting in nearly isomorphic variation among all traits in these lines. Single‐pair bottlenecks significantly disrupted the trait interrelationships, and the suites of traits identified by principal components of the additive genetic correlation and covariance matrices for the control population were no longer evident in these bottleneck lines. The alteration of the genetic relationships among traits as a result of a bottleneck suggests that nonadditive components of genetic variation affecting these traits were present in the control line. We discuss the implications of nonadditive gene action, particularly epistasis, for speciation via bottlenecks.
Evolution | 1995
Edwin H. Bryant; Lisa M. Meffert
Selection for increased morphometric shape (ratio of wing length to thorax width) was compared between control (nonbottlenecked) populations and bottlenecked populations founded with two male–female pairs of flies. Contrary to neutral expectation, selectional response was not reduced in bottlenecked populations, and the mean realized heritabilities and additive genetic variances were higher for the bottlenecked lines than for the nonbottlenecked lines. Additive genetic variances based on these realized heritabilities were consistent with independent estimates of genetic variances based on parent–offspring covariances. Joint scaling tests applied to the crosses between selected lines and their controls revealed significant nonadditive components of genetic variance in the ancestor, which were not detected in the crosses involving bottlenecked lines. The nonbottlenecked lines responded principally by changes in one trait or the other (wing length or thorax width) but not in both, and regardless of which trait responded, larger trait size was dominant and epistatic to smaller size. Stabilizing selection for morphometric shape in the ancestor likely molded the genetic architecture to include nonadditive genetic effects.
Heredity | 1996
Edwin H. Bryant; Lisa M. Meffert
The genetic architectures of four morphometric traits in the housefly, Musca domestica L., were analysed using a paternal half-sib design on a large outbred base population and on two populations each established with two pairs of flies from the base population. By including parents with the offspring in the analysis, phenotypic variance was subdivided into components for additive, dominance, additive-by-additive epistasis and environmental variation. In relation to the nonbottlenecked base population, narrow sense hertitability was lower in the bottle-necked populations, largely because of an increase in the level of the environmental component of variance. Averaged over the four traits in the nonbottlenecked base population, nonadditive components contributed nearly 60 per cent of the phenotypic variance, with more than half of this being attributable to epistasis. Two of the four traits showed reduced additive genetic variance in the bottlenecked lines, whereas two of the traits showed increased additive genetic variance. A major difference in the genetic architecture between traits showing these two disparate bottleneck effects was the presence of epistasis in the nonbottlenecked base population for the traits which showed an increase in the additive component. Overall, there was a significant positive relationship between the initial percentage contribution of epistasis in the base population and the gain in the additive component in the bottleneck lines, as predicted by models incorporating additive-by-additive epistasis.
Evolution | 1992
Lisa M. Meffert; Edwin H. Bryant
The extent of genome‐wide restructuring predicted in bottleneck models of speciation is addressed in assays of non‐reproductive behavior in lines of the housefly. After five serial founder‐flush cycles of one of three sizes (1, 4, or 16 pairs), each bottleneck line showed significant differentiation from the outbred control in ambulatory levels and grooming sequences in videotaped records of precopulatory activity. Only one line (4‐pair) showed overall lethargy which was associated to inbreeding depression in egg‐to‐adult viability, thus exemplifying a case of probable extinction due to bottlenecks. The two most hyperactive lines (1‐ and 16‐pair) showed very similar directions of differentiation from the control in locomotor activity and grooming behavior, as well as in mating behavior evaluated from a separate study. This high congruence suggested that directional selection toward the phenotypic optima of the ancestor operated on the bottleneck populations and that a 10‐fold difference in theoretical inbreeding coefficients did not affect the magnitude of response. The remaining two bottleneck lines showed some independence from these general trajectories, their divergence along minor axes of ancestral intercorrelation structure possibly being more important to the formation of new species. Significant perturbations of the thresholds for execution of grooming and locomotor movements suggested increased evolutionary potential for ritualization (i.e., sexual selection for adoption of non‐reproductive behavior into courtship repertoire) due to bottlenecks.
Evolution | 1996
Edwin H. Bryant; Lisa M. Meffert
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