Edwin H. Bryant

THE INFLUENCE OF VARIABLE RATES OF INBREEDING ON FITNESS, ENVIRONMENTAL RESPONSIVENESS, AND EVOLUTIONARY POTENTIAL

Abstract.— We manipulated experimental populations of the housefly (Musca domestica L.) under three inbreeding schemes (fast, slow, and punctuated) to partition out the influences of different means and variances in the rate of inbreeding, per generation, while controlling for the final level of inbreeding as a constant. One treatment used constant fast inbreeding (11% per generation; Ne= 4 for 4 generations), for a comparison to one that was consistently slow (3% per generation; Ne= 16 for 14 generations). The third followed a model for serial founder‐flush events. Each founder‐flush episode involved a one‐generation pulse of fast inbreeding (Ne= 4) followed by two generations of very low (or no) inbreeding, yielding high intergenerational variation (i.e., for an average inbreeding rate of 4% per generation). Allozyme assays showed that we achieved the intended final inbreeding coefficient of about 37%. All inbreeding schemes decreased fitness levels in terms of egg‐to‐adult viability, development time, and male mating success relative to the outbred control. The consistently fast inbreeding protocol had more pronounced reductions in fitness, relative to the other two inbreeding schemes. In comparison to the fast and punctuated regimes, the consistently slow protocol preserved evolutionary potential (as assayed by the genetic divergence of subpopulations exposed to different environments) in egg‐to‐adult viability, and (albeit anecdotally) reduced the extinction probabilities, especially in a novel environment. The punctuated treatment did not optimize the potential for purge as predicted, but instead reduced fitness, evolutionary potential, and environmental responsiveness (as measured by genotype‐by‐environment interactions). This founder‐flush treatment also had the highest extinction probabilities. Longer periods of population flush might be necessary to purge effectively in a punctuated scheme. We conclude that the rate of inbreeding, independent from the final level, can have important effects on population fitness, environmental responsiveness, and evolutionary potential.

Fitness, genetic load and purging in experimental populations of the housefly

The relative effects of purging of the genetic load versus thefixation of deleterious alleles, under inbreeding, will influencea populations probability of extinction. The relative contributionof these two phenomena is expected to depend upon the rate ofinbreeding. A further complication is due to the fact that a purgingof the genetic load in one environment does not necessarily implya purging of the genetic load in other environments. To addressthese two issues, we compare fitness and genetic load in populationsexperiencing similar levels of inbreeding, but occurring as either ashort-term bottleneck or as a consequence of long-term reducedpopulation size, over a range of environments. Inbred populationshave consistently lower fitness than outbred populations acrossall environments tested. However, the bottlenecked populationssuffer less inbreeding depression for a given level of inbreeding,whether or not challenged by novel environments, than populationskept at a constant small size. The results of this study demonstratethat populations initiated from a small number of founders are ableto recover fitness and survive novel environmental challenges,provided that habitat is available for rapid population growth.

The evolution of senescence under curtailed life span in laboratory populations of Musca domestica (the housefly)

The evolution of senescence may be explained by two different, but not mutually exclusive, genetic mechanisms. The antagonistic pleiotropy hypothesis predicts that senescence is a consequence of the fixation of alleles with pleiotropic effects favouring early life fitness, but bearing a cost in later life. The mutation-accumulation hypothesis attributes senescence to the accumulation of deleterious mutations with late-acting effects on fitness in mutation–selection balance. Experiments were carried out on the housefly, Musca domestica, in which large and small populations were maintained so that reproduction was limited to four or five days after reaching sexual maturity. Longevity declined significantly under the husbandry protocol and was largely the same in large and small populations; this is consistent with the random accumulation of deleterious alleles affecting longevity under curtailed life span, although laboratory adaptation cannot be ruled out entirely as a causal mechanism. An analysis of life-history data did not provide evidence for a trade-off between longevity and age at sexual maturity, developmental time, or dry body weight, but there was an apparent trade-off between longevity and early progeny production, in support of antagonistic pleiotropy.

Habitat selection in a variable environment.

Abstract A Monte Carlo simulation scheme was utilized to determine optimal strategies of habitat utilization in a variable environment. The model allows for differences in quality among habitats at any one time and for varying levels of environmental variance and autocorrelation. When habitats are on the average equal in quality, tracking of temporal fluctuations in environment through variable habitat selection is universally advantageous with the gain in fitness limited by environmental variance, autocorrelation, and number of available habitats. Average differences in quality among habitats will restrict the advantage of variable habitat utilization (over complete usage of the average better habitat) to cases of high environmental autocorrelation or high ratios of enviromental variance to mean habitat separation. Extending an earlier prediction of Levins (1965), the average heterozygosity per individual in a natural population should increase with increasing environmental variance.

QUANTITATIVE GENETIC ESTIMATES OF MORPHOMETRIC VARIATION IN WILD-CAUGHT AND LABORATORY-REARED HOUSEFLIES

Quantitative genetic estimates of morphometric traits in the housefly, Musca domestica L, were made on parents captured in the wild or reared in the laboratory. Phenotypic variation of morphometric traits declined within the laboratory, but as the additive genetic component of variation also declined, there was no net change in ∗∗∗narrow‐sense heritabilities of these traits across environments. Additive genetic variances were inflated only when wild‐caught females were used as parents, suggesting that a maternal effect was present.

Inbreeding and heterogamic mating: an alternative to Averhoff and Richardson.

An alternative explanation to the pheromonal control of mating through chemoreceptor saturation proposed by Averhoff and Richardson (1974) is offered for the apparent rise in heterogamic mating in their experiments, after several generations of full-sib mating. In a multiple-choice mating between two genotypic strains differing in their level of sexual vigor, there is a sequence from heterogamic to homogamic mating. It is proposed that, by reducing mating speed, inbreeding changes the rate of this sequence but not its pattern, so the apparent level of heterogamic mating will increase during inbreeding, for a fixed observation period. This hypothesis was tested using the Kence-Bryant model of mating success.

The effect of temporal advantage on competition between two strains of the housefly

This study reports the effect of temporal advantage on larval competition between two strains of the housefly. Temporal advantage herein refers to a head-start to one of two competing cohorts, where intra-cohort age variability is minimal. Such lack of synchrony can be contrasted with the simultaneous introduction of two larval cohorts differing in age distribution (e. g., see SOKAL, 1967; WOOL, 1969a). Laboratory analyses of competition between genetic strains of insects are generally initiated with equal aged eggs, larvae, or adults placed simultaneously in a closed environment. The effect of various factors, including strain proportion (SOKAL and KARTEN, 1963; SOKAL and HUBER, 1963; SCHLAGER, 1963; BHALLA and SOKAL, 1964; SULLIVAN and SOKAL, 1965), initial density (LEWONTIN, 1955; SOKAL and HUBER, 1963; SULLIVAN and SOKAL, 1963; BHALLA and SOKAL, 1964; SOKAL and KARTEN, 1964), size and shape of enclosure (WOOL, 1969b), and typ~ of food (BRooKES and FRAENKEL, 1958) are known to affect the outcome of competition as measured variously by percent survival to adulthood of the original cohort, mean dry weight of emerging adults, or length of the developmental period. Little attention has been given to the effect of temporal advantage on larval competition between immature cohorts. SANG (1949) studied mortality rates in successive cohorts of Drosophila larvae. He found that larvae in later batches tended to have lower survival rates, produce smaller adults, and take longer to complete development than larvae from earlier batches. The detrimental effect of later inoculation did not increase monotonically, however, for higher survival was found for larvae added on the second day than on the first day after initial inoculation. BAKKER (1969), also studying larval competition in Drosophila, concentrated on the head-start required by an inferior strain to equalize competitive ability in two competing cohorts, as reflected in weights of adult flies emerging from mixed cultures. The housefly has been studied extensively in our laboratory, describing the outcome of larval competition as a function of proportion and density of the competing genotypes (SULLIVAN and SOKAL, 1963; 1965; SOKAL and SULLIVAN, 1963; BHALLA and SOKAL, 1964; BRYANT and SOKAL, 1967, 1968; BRYANT, 1969). This study adds further to our basic understanding of the ecological genetics of the organism. However, the findings should be of wider interest inasmuch as compensatory head-starts

The role of medium conditioning in the population dynamics of the housefly

The role of larval medium conditioning on the behavior of larvae and of ovipositing adults of the housefly,Musca domestica L., was investigated through behavioral preference tests. Larvae were strongly attracted to medium conditioned by themselves or other larvae, while adult females overwhelmingly oviposited in fresh medium. Medium conditioning occurs within a few hours after hatching of an egg cohort and is effective in preventing overcrowding of a single site by shutting off further oviposition within 24 hours after eggs are initially deposited. A model of medium conditioning optimizes density for developing larvae and could also provide for regulation of local larval populations.

Differential Responses of Wild and Laboratory Strains of the Housefly to PCBs

Mixtures of polychlorinated biphenyls, Aroclor 1242 and 1254, had different effects on larval survival of strains of the housefly Musca domestica recently derived from nature, a long-established laboratory strain, and a strain selected for insecticide resistance. All strains tolerated high levels of PCBs; however, both wild-derived strains exhibited unexpected increased survival upon exposure to moderate levels of PCBs alone, whereas the long-established laboratory strain exhibited lowered larval survival in the presence of PCBs. This was not related to a lack of uptake of PCBs by the wild-derived flies, since uptake was high and all major Aroclor GC fractions were represented in the emerging flies. There was increased effectiveness of insecticides in the presence of PCBs on the long-established laboratory strain, but there was no such synergism with insecticides for the wild-derived flies. Recent evolutionary modification of the effects of PCBs alone or in conjunction with insecticides has apparently occurred in this species.

Obituary: David H. Reed (24 March 1963–24 October 2011)

David H. Reed, an Associate Editor of Conservation Genetics, passed away suddenly on 24 October 2011, at age 48 from heart failure. David is survived by his wife Rasita and daughter Vanessa (6 years of age), his mother and three brothers. David was an outstanding scientist who achieved a great deal in a scientific career post-PhD of only 13 years. He had 47 published papers (with more to come), and has been cited 1755 times (ISI Web of Knowledge 19 Dec 2011). David was a highly valued Associate Editor for Conservation Genetics (2005–2011), an Associate Editor (2007–2010) and then Editor (from 2010) of Animal Conservation, and an Associate Editor of Journal of Wildlife Thailand (from 2011). David was born in Mount Holly, New Jersey to parents of modest means, a situation worsened by his father’s death at 46, also from heart failure. He completed a BBA in economics and statistics at Lincoln Memorial University in Tennessee in 1988. David joined the military and completed several years of service, which assisted him in obtaining his college and graduate education. Below we highlight his most novel and important scientific contributions.