Correlated responses to selection for faster development and early reproduction in Drosophila: the evolution of larval traits

Studies on selection for faster development in Drosophila have typically focused on the trade-offs among development time, adult weight, and adult life span. Relatively less attention has been paid to the evolution of preadult life stages and behaviors in response to such selection. We have earlier reported that four laboratory populations of D. melanogaster selected for faster development and early reproduction, relative to control populations, showed considerably reduced preadult development time and survivorship, dry weight at eclosion, and larval growth rates. Here we study the larval phase of these populations in greater detail. We show here that the reduction in development time after about 50 generations of selection is due to reduced duration of the first and third larval instars and the pupal stage, whereas the duration of the second larval instar has not changed. About 90% of the preadult mortality in the selected populations is due to larval mortality. The third instar larvae, pupae, and freshly eclosed adults of the selected populations weigh significantly less than controls, and this difference appears during the third larval instar. Thereafter, percentage weight loss during the pupal stage does not differ between selected and control populations. The minimum amount of time a larva must feed to subsequently complete development is lower in the selected populations, which also exhibit a syndrome of reduced energy expenditure through reduction in larval feeding rate, larval digging and foraging activity, and pupation height. Comparison of these results with those observed earlier in populations selected for adaptation to larval crowding and faster development under a different protocol from ours reveal differences in the evolved traits that suggest that the responses to selection for faster development are greatly affected by the larval density at which selection acts and on details of the selection pressures acting on the timing of reproduction.     

K-selection, α-selection, effectiveness, and tolerance in competition: Density-dependent selection revisited

In the Drosophila literature, selection for faster development and selection for adapting to high density are often confounded, leading, for example, to the expectation that selection for faster development should also lead to higher competitive ability. At the same time, results from experimental studies on evolution at high density do not agree with many of the predictions from classical density-dependent selection theory. We put together a number of theoretical and empirical results from the literature, and some new experimental results on Drosophila populations successfully subjected to selection for faster development, to argue for a broader interpretation of density-dependent selection. We show that incorporating notions of alpha-selection, and the division of competitive ability into effectiveness and tolerance components, into the concept of density-dependent selection yields a formulation that allows for a better understanding of the empirical results. We also use this broader formulation to predict that selection for faster development in Drosophila should, in fact, lead to the correlated evolution of decreased competitive ability, even though it does lead to the evolution of greater efficiency and higher population growth rates at high density when in monotypic culture.     

Density-dependent natural selection inDrosophila: Trade-offs between larval food acquisition and utilization

Summary Natural selection at high densities has often been postulated to favour the evolution of greater efficiency of food use. Contrary to this expectation, a previous study suggested the existence of a trade-off between larval feeding rate and efficiency at using food to complete larval development in populations ofDrosophila melanogaster subjected to crowding for many generations. In this paper, we confirm the generality of such a density-dependent trade-off between food acquisition and utilization by demonstrating its occurrence in a new set ofDrosophila populations subjected to extreme larval crowding. We suggest that such trade-offs between food acquisition and food use may represent a general phenomenon in organisms exhibiting scramble competition. We test and reject the possible mechanistic explanation that decreased efficiency of food use in faster-feeding larvae may merely be a consequence of a faster passage of food through the gut, leading to incomplete assimilation of nutrients and energy.     

The devil in the details of life-history evolution: Instability and reversal of genetic correlations during selection on<Emphasis Type="Italic">Drosophila</Emphasis> development

The evolutionary relationships between three major components of Darwinian fitness, development rate, growth rate and preadult survival, were estimated using a comparison of 55 distinct populations ofDrosophila melanogaster variously selected for age-specific fertility, environmental-stress tolerance and accelerated development. Development rate displayed a strong net negative evolutionary correlation with weight at eclosion across all selection treatments, consistent with the existence of a size-versus-time tradeoff between these characters. However, within the data set, the magnitude of the evolutionary correlation depended upon the particular selection treatments contrasted. A previously proposed tradeoff between preadult viability and growth rate was apparent only under weak selection for juvenile fitness components. Direct selection for rapid development led to sharp reductions in both growth rates and viability. These data add to the mounting results from experimental evolution that illustrate the sensitivity of evolutionary correlations to (i) genotype-by-environment (G X E) interaction, (ii) complex functional-trait interactions, and (iii) character definition. Instability, disappearance and reversal of patterns of genetic covariation often occur over short evolutionary time frames and as the direct product of selection, rather than some stochastic process. We suggest that the functional architecture of fitness is a rapidly evolving matrix with reticulate properties, a matrix that we understand only poorly.     

Phenotypic evolution in stochastic environments: The contribution of frequency- and density-dependent selection

Understanding how environmental variation affects phenotypic evolution requires models based on ecologically realistic assumptions that include variation in population size and specific mechanisms by which environmental fluctuations affect selection. Here we generalize quantitative genetic theory for environmentally induced stochastic selection to include general forms of frequency- and density-dependent selection. We show how the relevant fitness measure under stochastic selection relates to Fisher's fundamental theorem of natural selection, and present a general class of models in which density regulation acts through total use of resources rather than just population size. In this model, there is a constant adaptive topography for expected evolution, and the function maximized in the long run is the expected factor restricting population growth. This allows us to generalize several previous results and to explain why apparently “-selected” species with slow life histories often have low carrying capacities. Our joint analysis of density- and frequency-dependent selection reveals more clearly the relationship between population dynamics and phenotypic evolution, enabling a broader range of eco-evolutionary analyses of some of the most interesting problems in evolution in the face of environmental variation.     

Divergent selection drives the adaptive radiation of crossbills

Abstract Knowledge of how phenotype influences fitness is necessary if we are to understand the basis of natural selection and how natural selection contributes to adaptive radiations. Here I quantify selection on a wild population of red crossbills ( Loxia curvirostra complex) in the South Hills, Idaho. Bill depth is the target of selection and selection on bill depth is stabilizing. I then show how fitness is related to both bill depth and performance. I use these and previously published relationships to estimate a fitness surface for five species of red crossbills that are part of an ongoing adaptive radiation in western North America. The fitness surface for crossbills has distinct peaks and valleys, with each crossbill species residing on or very near the summits. This work strongly supports a key tenet of the ecological theory of adaptive radiations; namely, divergent selection for utilizing alternative resources is the ultimate cause of adaptive radiations.     

Norms of reaction and diversifying selection

The numbers of progeny produced by comparable numbers of female Drosophila melanogaster of 26 geographic strains on nine different culture media are examined in the context of norms of reaction. Having emphasized that diversifying selection is seldom discussed simultaneously with its seemingly related topic, norms of reaction, I present the following argument: diversifying selection has generally been viewed as involving sub-populations inhabiting separate localities and subject to different patterns of selection, norms of reaction as variation whose weighted average determines the relative fitnesses of different genotypes within individual sub-populations. Should environmental challenges frequently involve life or death (including sterility) outcomes, norms of reaction involving components of fitness engender diversifying selection within local populations (demes).     

Circadian clocks and life-history related traits: Is pupation height affected by circadian organization in<Emphasis Type="Italic">Drosophila melanogaster</Emphasis>?

InD. melanogaster, the observation of greater pupation height under constant darkness than under constant light has been explained by the hypothesis that light has an inhibitory effect on larval wandering behaviour, preventing larvae from crawling higher up the walls of culture vials prior to pupation. If this is the only role of light in affecting pupation height, then various light : dark regimes would be predicted to yield pupation heights intermediate between those seen in constant light and constant darkness. We tested this hypothesis by measuring pupation height under various light : dark regimes in four laboratory populations ofDrosophila melanogaster. Pupation height was the greatest in constant darkness, intermediate in constant light, and the least in a light/dark regime of LD 14:14 h. The results clearly suggest that there is more to light regime effects on pupation height than mere behavioural inhibition of wandering larvae, and that circadian organization may play some role in determining pupation height, although the details of this role are not yet clear. We briefly discuss these results in the context of the possible involvement of circadian clocks in life-history evolution.     

Indirect thermal selection in Drosophila melanogaster and adaptive consequences

Summary Short-term indirect selection in Drosophila melanogaster for heat-sensitivity and heat resistance resulted in two strains, one heat sensitive and another heat resistant, and correlated responses were found for the rate of heat shock protein synthesis, behavioral patterns (asymmetrical sexual isolation) and fitness components (fecundity, fertility, viability, developmental time), as well as for several enzyme activities (MDH, G-6-PDH, ADH, ACHE). These responses associated with temperature selection may reflect the effects of differential inbreeding depression caused by homozygosity of temperature sensitive mutations with different pleiotropic effects. Selection even of a very short duration can induce significant adaptive and evolutionary changes.     

Effects on ADH activity and distribution,following selection for tolerance to ethanol in Drosophila melanogaster

Strains of Drosophila melanogaster homozygous for either the Adh ^F or the Adh ^S allele were kept on food supplemented with ethanol for 20 generations. These strains (FE and SE) were tested for tolerance to ethanol and compared with control strains (FN and SN). The E strains showed increased tolerance to ethanol both in the adult and in the juvenile life stages. In adults the increase in tolerance was not accompanied by an increase in overall ADH activity. However, there were changes in the distribution of ADH over the body parts. Flies of the FE strain possessed significantly more ADH in the abdomen, compared with FN. Another set of FN and SN populations were started both on standard food and on ethanol food with reduced yeast concentrations. After 9 months ADH activities were determined in flies from these populations which had been placed on three different media: the food the populations had been kept on, regular food and regular food supplemented with ethanol. The phenotypic effects of yeast reduction on ADH activity were considerably, but longterm genetic effects were limited.     

Reproductive fitness and artificial selection in animal breeding: culling on fitness prevents a decline in reproductive fitness in lines of Drosophila melanogaster selected for increased inebriation time

Summary The maintenance of reproductive fitness in lines subjected to artificial selection is one of the major problems in animal breeding. The decline in reproductive performance has neither been predictable from heritabilities and genetic correlations, nor have conventional selection indices been adequate to avoid the problem. Gowe (1983) has suggested that the heritabilities of reproductive traits are non-linear, with heritabilities being higher on the lower fitness side. Consequently, he has predicted that culling on reproductive fitness in artificial selection lines will be effective in preventing the usual declines in fitness. An experimental evaluation of Gowe's prediction has been carried out by comparing fitnesses of replicated lines of three treatments: selection for increased inebriation time without culling on fitness (HO), selection for inebriation time with culling of 20% (4/20) of selected females on reproductive fitness (HS), and unselected controls (C). Response to selection for inebriation time in the two selection treatments was similar. After 25 generations, the competitive index, a measure of reproductive fitness, was significantly lower in the HO treatment than the HS treatment, while the HS treatment did not differ from the control lines or the base population. These results demonstrate for the first time that culling on reproductive fitness in selection lines can be used to prevent the usual decline in reproductive performance.     

An approach to study the evolution of theDrosophila 5S ribosomal genes using P-element transformation

Summary The P-element-mediated gene transfer system was used to introduceDrosophila teissieri 5S genes into theDrosophila melanogaster genome. Eight transformedD. melanogaster strains that carryD. teissieri 5S mini-clusters consisting of 9–21 adjacent 5S units were characterized. No genetic exchanges betweenD. melanogaster andD. teissieri 5S clusters were detected over a 2-year survey of the eight strains. The occurrence of small rearrangements within theD. melanogaster 5S cluster was demonstrated in one of the transformed strains.     

The Genomic Architecture of Adaptation to Larval Malnutrition Points to a Trade-off with Adult Starvation Resistance in Drosophila

Periods of nutrient shortage impose strong selection on animal populations. Experimental studies of genetic adaptation to nutrient shortage largely focus on resistance to acute starvation at adult stage; it is not clear how conclusions drawn from these studies extrapolate to other forms of nutritional stress. We studied the genomic signature of adaptation to chronic juvenile malnutrition in six populations of Drosophila melanogaster evolved for 150 generations on an extremely nutrient-poor larval diet. Comparison with control populations evolved on standard food revealed repeatable genomic differentiation between the two set of population, involving >3,000 candidate SNPs forming >100 independently evolving clusters. The candidate genomic regions were enriched in genes implicated in hormone, carbohydrate, and lipid metabolism, including some with known effects on fitness-related life-history traits. Rather than being close to fixation, a substantial fraction of candidate SNPs segregated at intermediate allele frequencies in all malnutrition-adapted populations. This, together with patterns of among-population variation in allele frequencies and estimates of Tajima’s D, suggests that the poor diet results in balancing selection on some genomic regions. Our candidate genes for tolerance to larval malnutrition showed a high overlap with genes previously implicated in acute starvation resistance. However, adaptation to larval malnutrition in our study was associated with reduced tolerance to acute adult starvation. Thus, rather than reflecting synergy, the shared genomic architecture appears to mediate an evolutionary trade-off between tolerances to these two forms of nutritional stress.     

Sure facts, speculations, and open questions about the evolution of transposable element copy number

Transposable elements (TEs) are sequences capable of multiplying in their host's genome. They survive by increasing copy numbers due to transpositions, and natural selection washes them out because hosts with heavier loads of TEs have lower fitness. The available phylogenetic evidence supports the view that TEs have existed in living organisms for hundreds of millions of years. A fundamental question facing the field is how can an equilibrium be attained between transposition and selection which allows these parasitic genetic elements to persist for such a long time period? To answer this question, it is necessary to understand how the rate of TE transposition is controlled and to describe the mechanisms with which natural selection opposes TE accumulation. Perhaps the best models for such a study are copia and gypsy retrotransposons in Drosophila. Their average rate of transposition in nature is between 10^?5 ? 10^?4 transpositions per copy per generation. Unlike nature, transposition rates vary widely, from zero to 10^?2, between laboratory lines. This variability in transposition rate is controlled by host genes. It is probable that in nature TE site heterogeneity is caused by frequent transpositions in rare flies with permissive alleles, and no transpositions happen in the rest of flies. The average rate of TE transposition in nature may thus depend on the frequency of permissive alleles, which is a function of the rate of mutation from restrictive to permissive alleles, the mechanism and the strength of selection opposing TE multiplication, and population size. Thus, evolution of the frequency of permissive alleles of genes controlling transposition must be accounted for to understand evolution of TE copy numbers.     

Correlated responses to selection for wing length in allozyme systems of Drosophila melanogaster

Summary Significant changes of genotypic structure in 20 lines selected for wing length are detected by analysis of the allelic frequencies of several enzyme loci (XDH, LAP-D, EST-6, 1-APH, ADH, -GPDH). These changes are not haphazard but a consequence of the effects of selection on the genetic structure of the population, since replicate lines always behave in a parallel way. The changes are larger in the lines selected for short wings, in which the genetic variability decreases considerably. This decrease is the result of selection for homozygosity, detected at the allozyme loci, but most probably reflects homozygosity of more or less extended chromosomal segments. Selection for wing length, especially for short wings, favoured recombinants of the initial founder chromosomes. Only in the 1-APH and the EST-6 loci, separated by 11.7 centimorgans on the genetic map, do the alleles linked in the founder lines change in parallel in the control and long wing lines. The correlated response in the allozyme allele frequencies cannot be accounted for by a direct influence of the allozymes on the variability in wing length. The changes in the EST-6, 1-APH and perhaps in the LAP-D, can be explained by a direct effect of natural selection on the allozyme loci, probably in interaction with the effect of selection for wing length on linked loci. This last effect seems to be the main factor contributing to the change detected in the XDH locus.     

Effects on heterozygosity and reproductive fitness of inbreeding with and without selection on fitness in Drosophila melanogaster

The effects of inbreeding, with (IS) and without selection (IO) for reproductive fitness, on inbreeding depression and heterozygosity were evaluated in 20 lines of each treatment inbred over seven generations using full-sib mating. The survival of lines was significantly greater in IS (20/20) than in IO (15/20). The competitive index measure of reproductive fitness was significantly lower in the inbred lines than in the outbred base population, but not significantly different in surviving IS and IO lines. There was a trend for higher fitness in the IS treatment as relative fitnesses were 19% higher in IS than IO for surviving lines and 59% higher for all lines. Heterozygosities were lower in the inbred lines than in the base population, and significantly higher in the IS than the IO lines. Consequently, the reduction of inbreeding depression in IS has been achieved, at least in part, by slowing the rate of fixation.     

A Genomic Comparison of Faster-Sex, Faster-X, and Faster-Male Evolution Between Drosophila melanogaster and Drosophila pseudoobscura

A genomic comparison of Drosophila melanogaster and Drosophila pseudoobscura provides a unique opportunity to investigate factors involved in sequence divergence. The chromosomal arrangements of these species include an autosomal segment in D. melanogaster which is homologous to part of the X chromosome in D. pseudoobscura. Using orthologues to calculate rates of nonsynonymous (d_N) substitutions, we found genes on the X chromosome to be significantly more diverged than those on the autosomes, but it is not true for segment 3L-XR which is autosomal in D. melanogaster (3L) and X-linked in D. pseudoobscura (XR). We also found that the median d_N values for genes having reproductive functions in either the male, the female, or both sexes are higher than those for sequences without reproductive function and even higher for sequences involved in male-specific function. These estimates of divergence for male sex-related sequences are most likely underestimates, as the very rapidly evolving reproductive genes would tend to lose homology sooner and thus not be included in the comparison of orthologues. We also noticed a high proportion of male reproductive genes among the othologous genes with the highest rates of d_N. Reproductive genes with and without an orthologue in D. pseudoobscura were compared among D. melanogaster, D. simulans, and D. yakuba and it was found that there were in fact higher rates of divergence in the group without a D. pseudoobscura orthologue. These results, from widely separated taxa, bolster the thesis that sexual system genes experience accelerated rates of change in comparison to nonsexual genes in evolution and speciation. [Reviewing Editor: Dr. Willie J. Swanson]