Genomic differentiation between temperate and tropical Australian populations of Drosophila melanogaster

Determining the genetic basis of environmental adaptation is a central problem of evolutionary biology. This issue has been fruitfully addressed by examining genetic differentiation between populations that are recently separated and/or experience high rates of gene flow. A good example of this approach is the decades-long investigation of selection acting along latitudinal clines in Drosophila melanogaster. Here we use next-generation genome sequencing to reexamine the well-studied Australian D. melanogaster cline. We find evidence for extensive differentiation between temperate and tropical populations, with regulatory regions and unannotated regions showing particularly high levels of differentiation. Although the physical genomic scale of geographic differentiation is small--on the order of gene sized--we observed several larger highly differentiated regions. The region spanned by the cosmopolitan inversion polymorphism In(3R)P shows higher levels of differentiation, consistent with the major difference in allele frequencies of Standard and In(3R)P karyotypes in temperate vs. tropical Australian populations. Our analysis reveals evidence for spatially varying selection on a number of key biological processes, suggesting fundamental biological differences between flies from these two geographic regions.     

Reproductive asynchrony and population divergence between two tropical bird populations

High-latitude vertebrates generally breed seasonally and synchronouslyas the primary environmental cue used to time seasonal processesis photoperiod. Investigations of tropical vertebrates havealso documented seasonal reproduction, but it is unclear howsynchronous reproduction is, both within and between populations.In this study, we investigated whether seasonal reproductionin a tropical species is synchronous between two populationsin close proximity and, if not, whether asynchrony is correlatedwith genetic and cultural differentiation. We describe two equatorialpopulations of rufous-collared sparrows (Zonotrichia capensis),at the same latitude and separated by 25 km, that each breedseasonally but out of phase with each other. This asynchronousreproductive phenology is associated with local weather patternsand is independent of photoperiod. At a finer scale, reproductivetiming is more highly synchronized within monogamous pairs thanwithin the population as a whole. Associated with the differencein reproductive phenologies, we document that males in eachpopulation sing different song dialects. Using microsatelliteDNA analysis, we found limited gene flow and significant geneticdifferentiation between the two populations. From these resultswe hypothesize that cultural and genetic differentiation betweenpopulations, which can be greater in tropical populations thantemperate ones, can be associated with locally adapted reproductivephenologies.     

Phenotypic plasticity of sternopleural bristle number in temperate and tropical populations of Drosophila melanogaster

We investigated the phenotypic plasticity of sternopleural bristle (SB) number as a function of growth temperature in isofemale lines from temperate (France) and tropical (Congo) populations of Drosophila melanogaster. We found concave reaction norms with a maximum in the middle of the thermal range, except in four African lines which exhibited a regularly decreasing response curve. Genetic variability (intraclass correlation) and evolvability (genetic CV, coefficient of variation) were independent properties and did not change with temperature. Residual, within-line variability was, however, strongly influenced by growth temperature, showing a U-shaped response curve and a minimum CV of 9% at 21.5 degrees C. As expected from a previously known latitudinal cline, maximum values (MV) were higher in temperate than in tropical flies. The temperature of maximum value (TMV) was observed at a higher temperature in the tropical population, in agreement with similar adaptive trends already observed for other quantitative traits. Significant negative correlations within each population were observed between a plasticity curvature parameter and MV or TMV. No difference in curvature was, however, observed between populations, in spite of their very different MVs.     

Preference for ethanol in feeding and oviposition in temperate and tropical populations of Drosophila melanogaster

The natural habitat of Drosophila melanogaster Meigen (Diptera: Drosophilidae) is fermenting fruits, which can be rich in ethanol. For unknown reasons, temperate populations of this cosmopolitan species have higher ethanol resistance than tropical populations. To determine whether this difference is accompanied by a parallel difference in preference for ethanol, we compared two European and two tropical African populations in feeding and oviposition preference for ethanol‐supplemented medium. Although females of all populations laid significantly more eggs on medium with ethanol than on control medium, preference of European females for ethanol increased as ethanol concentration increased from 2 to 6%, whereas that of African females decreased. In feeding tests, African females preferred control medium over medium with 4% ethanol, whereas European females showed no preference. Males of all populations strongly preferred control medium. The combination of preference for ethanol in oviposition, and avoidance or neutrality in feeding, gives evidence that adults choose breeding sites with ethanol for the benefit of larvae, rather than for their own benefit. The stronger oviposition preference for ethanol of temperate than tropical females suggests that this benefit may be more important in temperate populations. Two possible benefits of ethanol for which there is some experimental evidence are cryoprotection and protection against natural enemies.     

Divergence of reaction norms of size characters between tropical and temperate populations of Drosophila melanogaster and D. simulans

Reaction norms to growth temperature of two size-related traits, wing and thorax length, were compared in tropical (West Indies) and temperate (France) populations of the two sibling species, Drosophila melanogaster and D. simulans. A major body size difference was found in D. melanogaster, with much smaller Caribbean flies, while D. simulans exhibited little size variation between geographical populations. The concave norms of reaction were adjusted to second- or third-degree polynomials, and characteristic points calculated i.e. maximum value (MV) and temperature of maximum value (TMV). TMVs were confirmed to be higher for thorax than for wing length, higher in D. melanogaster than in D. simulans, and higher in females than in males. For both traits Caribbean populations exhibited higher TMVs in the two species, strongly suggesting an adaptive shift of the reaction norms toward higher temperature in warm-adapted populations. The wing/thorax ratio was also analysed, and found to be significantly lower in tropical populations of both species. This ratio, which is related to wing loading and flight capacity, might evolve independently of body weight itself.     

Latitudinal variability of Drosophila melanogaster: allozyme frequencies divergence between European and Afrotropical populations

Allelic frequencies at five polymorphic loci were determined in seven European and six Afrotropical populations of Drosophila melanogaster. African populations, which may be considered as ancestral for the species, showed a greater genetic diversity as measured by the number of alleles found. Within each geographic group (Europe or tropical Africa) genetic distances between local populations were very small (D = 0.027). By contrast, the average distance between European and African populations (D = 0.389) was more than 12 times bigger. It was previously known that various morphological or physiological differences, which probably reflect genetic adaptations to different environments, exist between these temperate and tropical populations. Data presented here suggest that the divergence in allozyme frequencies also reflects some selective mechanisms.     

Latitudinal variability of Drosophila melanogaster: Allozyme frequencies divergence between European and Afrotropical populations

Allelic frequencies at five polymorphic loci were determined in seven European and six Afrotropical populations of Drosophila melanogaster. African populations, which may be considered as ancestral for the species, showed a greater genetic diversity as measured by the number of alleles found. Within each geographic group (Europe or tropical Africa) genetic distances between local populations were very small (D=0.027). By contrast, the average distance between European and African populations (D=0.389) was more than 12 times bigger. It was previously known that various morphological or physiological differences, which probably reflect genetic adaptations to different environments, exist between these temperate and tropical populations. Data presented here suggest that the divergence in allozyme frequencies also reflects some selective mechanisms.     

Disparate patterns of thermal adaptation between life stages in temperate vs. tropical Drosophila melanogaster

Many terrestrial ectothermic species exhibit limited variation in upper thermal tolerance across latitude. However, these trends may not signify limited adaptive capacity to increase thermal tolerance in the face of climate change. Instead, thermal tolerance may be similar among populations because behavioural thermoregulation by mobile organisms or life stages may buffer natural selection for thermal tolerance. We compared thermal tolerance of adults and embryos among natural populations of Drosophila melanogaster from a broad range of thermal habitats around the globe to assess natural variation of thermal tolerance in mobile vs. immobile life stages. We found no variation among populations in adult thermal tolerance, but embryonic thermal tolerance was higher in tropical strains than in temperate strains. We further report that embryos live closer to their upper thermal limits than adults – that is, thermal safety margins are smaller for embryos than adults. F1 hybrid embryos from crosses between temperate and tropical populations had thermal tolerance that matched that of tropical embryos, suggesting the dominance of heat‐tolerant alleles. Together, our findings suggest that thermal selection has led to divergence in embryonic thermal tolerance but that selection for divergent thermal tolerance may be limited in adults. Further, our results suggest that thermal traits should be measured across life stages to better predict adaptive limits.     

Dynamics of genetic rescue in inbred Drosophila melanogaster populations

Genetic rescue has been proposed as a management strategy to improve the fitness of genetically eroded populations by alleviating inbreeding depression. We studied the dynamics of genetic rescue in inbred populations of Drosophila. Using balancer chromosomes, we show that the force of heterosis that accompanies genetic rescue is large and allows even a recessive lethal to increase substantially in frequency in the rescued populations, particularly at stress temperatures. This indicates that deleterious alleles present in the immigrants can increase significantly in frequency in the recipient population when they are in linkage disequilibrium with genes responsible for the heterosis. In a second experiment we rescued eight inbred Drosophila populations with immigrants from two other inbred populations and observe: (i) there is a significant increase in viability both 5 and 10 generations after the rescue event, showing that the increase in fitness is not transient but persists long-term. (ii) The lower the fitness of the recipient population the larger the fitness increase. (iii) The increase in fitness depends significantly on the origin of the rescuers. The immigrants used were fixed for a conditional lethal that was mildly deleterious at 25°C but lethal at 29°C. By comparing fitness at 25°C (the temperature during the rescue experiment) and 29°C, we show that the lethal allele reached significant frequencies in most rescued populations, which upon renewed inbreeding became fixed in part of the inbred lines. In conclusion, in addition to the fitness increase genetic rescue can easily result in a substantial increase in the frequency of mildly deleterious alleles carried by the immigrants. This can endanger the rescued population greatly when it undergoes recurrent inbreeding. However, using a sufficient number of immigrants and to accompany the rescue event with the right demographic measures will overcome this problem. As such, genetic rescue still is a viable option to manage genetically eroded populations.     

Quantitative genetic differences between populations of Drosophila melanogaster from diverse geographic origins

Crosses were made between each seven populations of Drosophila melanogaster-three of which were laboratory populations and four were recently captured populations-and a line previously selected for low sternopleural bristle number for many generations. In each of six replicate lines from each cross, selection was practised for low sternopleural bristle number; subsequently these replicates were intercrossed and reselected. Introduction of new genetic material from four populations into the selected line was achieved, indicating the presence in these populations of particular alleles which are absent from or rare in the base populations of the selected line. Introduction of new genetic material from three populations into the selected line was not achieved. Consequently, it was possible to establish two groups of populations. In each group, the populations appear to be segregating for essentially the same alleles. Differences in gene frequency rather than the presence or absence of particular alleles are mainly responsible for the differences observed between the populations.In all, 11 populations screened for genetic differences controlling sternopleural bristle number. There are widespread genetic similarities among populations of very different geographic origin. Laboratory populations as a group are not more homogeneous than recently collected populations, although the latter are genetically more variable. Drift alone could account for the reduction of variability in the laboratory populations.     

Reproductive diapause and life-history clines in North American populations of Drosophila melanogaster

Latitudinal clines are widespread in Drosophila melanogaster, and many have been interpreted as adaptive responses to climatic variation. However, the selective mechanisms generating many such patterns remain unresolved, and there is relatively little information regarding how basic life-history components such as fecundity, life span and mortality rates vary across environmental gradients. Here, it is shown that four life-history traits vary predictably with geographic origin of populations sampled along the latitudinal gradient in the eastern United States. Although such patterns are indicative of selection, they cannot distinguish between the direct action of selection on the traits in question or indirect selection by means of underlying genetic correlations. When independent suites of traits covary with geography, it is therefore critical to separate the widespread effects of population source from variation specifically for the traits under investigation. One trait that is associated with variation in life histories and also varies with latitude is the propensity to express reproductive diapause; diapause expression has been hypothesized as a mechanism by which D. melanogaster adults overwinter, and as such may be subject to strong selection in temperate habitats. In this study, recently derived isofemale lines were used to assess the relative contributions of population source and diapause genotype in generating the observed variance for life histories. It is shown that although life span, fecundity and mortality rates varied predictably with geography, diapause genotype explained the majority of the variance for these traits in the sampled populations. Both heat and cold shock resistance were also observed to vary predictably with latitude for the sampled populations. Cold shock tolerance varied between diapause genotypes and the magnitude of this difference varied with geography, whereas heat shock tolerance was affected solely by geographic origin of the populations. These data suggest that a subset of life-history parameters is significantly influenced by the genetic variance for diapause expression in natural populations, and that the observed variance for longevity and fecundity profiles may reflect indirect action of selection on diapause and other correlated traits.     

Temperature-related divergence in experimental populations of Drosophila melanogaster. II. Correlation between fitness and body dimensions

From a laboratory stock of Drosophila melanogaster (Oregon), reared for more than 20 years at 18° C, a new population was derived and maintained at 28° C for 8 years. The chromosomal and cytoplasmic contribution to genetic divergence between the two populations was estimated. Six body traits and reproductive fitness were taken into account. The third chromosome is responsible for the adaptive difference for temperature between the two lines. Temperature-selected genes which control body size are located on the second and third chromosomes, although the contribution of each chromosome depends on the environment in which the flies develop. The correlation between the chromosomal and cytoplasmic contributions to different traits and fitness, changes with temperature. At 28° C the correlation between fitness and each body trait is proportional to the response to selection exhibited by each of them, but this is not true at 18° C. Body size has, therefore, an adaptive significance in relation to temperature, which is expressed only in the environment where selection occurs. Cytoplasmic genes affect almost all characters to an extent similar to that of chromosomal genes. Inter-chromosomal and nucleo-cytoplasmic interactions are present and also change with temperature. In general, genes selected in a given environment produce greater phenotypic changes in that environment than in another. The population that experienced both temperatures is fitter in both environments, suggesting that the capacity to adapt to warm temperatures depends on genes other than those which are involved in the adaptation to cold.     

Mitochondrial DNA variation and genetic structure in populations of Drosophila melanogaster

The understanding of the genetic structure of a species can be improved by considering together data from different types of genetic markers. In the past, a number of worldwide populations of Drosophila melanogaster have been extensively studied for several such markers, including allozymes, chromosomal inversions, and quantitative characters. Here we present results from a study of restriction- fragment-length polymorphisms of mitochondrial DNA (mtDNA) in 92 isofemale lines from many of the same geographic populations of D. melanogaster. Eleven restriction enzymes were used, of which four revealed restriction-site polymorphism. A total of 24 different haplotypes were observed, of which 18 were unique to single populations. In many populations, the unique haplotypes have reached high frequency without being observed in neighboring populations. A Wagner parsimony tree reveals that mutationally close variants show geographical clumping, suggesting local differentiation of mtDNA in populations. The Old-World and the New-World populations are differentiated, with the predominant Old-World haplotype being virtually absent from the New World. These results contrast with those for the nuclear genes, in which many loci show parallel clines in different continents, and suggest a common origin of D. melanogaster populations in North America.      

Reproductive isolation in natural populations of Drosophila melanogaster from Brazzaville (Congo)

The aim of this work is to analyze the homogamy previously detected between two natural populations of Drosophila melanogaster from Brazzaville. It is shown that mating isolation was still maintained under laboratory conditions 10 years after the populations samples were trapped. Isolation seemed to be due mainly to pre-mating isolation and we checked for any suggestion of post-mating mortality of hybrids. Pre-mating isolation was not symmetrical, and significant ² values were found in 3/4 possible 3-way mating choice experiments. The only exception involved a male from the countryside and two females (one from each population) for which no significant mating preference was detected. Mortality of hybrids was intermediate between those of the parental strains showing a clear maternal effect and the existence of partial dominance. Major differences in the cuticular hydrocarbons were also found and they could account for the isolation. These findings in populations from African breweries indicate that they are closely related to European ones, suggesting that this phenomenon is not a case of sympatric speciation, but probably attributable to the reintroduction of an allopatric population.     

Stability of genetic parameters in Drosophila melanogaster populations from Odessa city

The dynamics of allele frequency of the carboxiesterase gene, the frequency of sex-linked lethal mutations, and recombination events in natural populations of Drosophila melanogaster from Odesa were studied. All studied estimates were shown to remain unchanged in June, July, and August during the 2009 collection season.