The genetic basis of adaptive pigmentation variation in Drosophila melanogaster

In a broad survey of Drosophila melanogaster population samples, levels of abdominal pigmentation were found to be highly variable and geographically differentiated. A strong positive correlation was found between dark pigmentation and high altitude, suggesting adaptation to specific environments. DNA sequence polymorphism at the candidate gene ebony revealed a clear association with the pigmentation of homozygous third chromosome lines. The darkest lines sequenced had nearly identical haplotypes spanning 14.5 kb upstream of the protein-coding exons of ebony. Thus, natural selection may have elevated the frequency of an allele that confers dark abdominal pigmentation by influencing the regulation of ebony.     

Genetic mapping of adaptive wing size variation in Drosophila simulans

Many ecologically important traits exhibit latitudinal variation. Body size clines have been described repeatedly in insects across multiple continents, suggesting that similar selective forces are shaping these geographical gradients. It is unknown whether these parallel clinal patterns are controlled by the same or different genetic mechanism(s). We present here, quantitative trait loci (QTL) analysis of wing size variation in Drosophila simulans. Our results show that much of the wing size variation is controlled by a QTL on Chr 3L with relatively minor contribution from other chromosome arms. Comparative analysis of the genomic positions of the QTL indicates that the major QTL on Chr 3 are distinct in D. simulans and D. melanogaster, whereas the QTL on Chr 2R might overlap between species. Our results suggest that parallel evolution of wing size clines could be driven by non-identical genetic mechanisms but in both cases involve a major QTL as well as smaller effects of other genomic regions.     

A comprehensive assessment of geographic variation in heat tolerance and hardening capacity in populations of Drosophila melanogaster from eastern Australia

We examined latitudinal variation in adult and larval heat tolerance in Drosophila melanogaster from eastern Australia. Adults were assessed using static and ramping assays. Basal and hardened static heat knockdown time showed significant linear clines; heat tolerance increased towards the tropics, particularly for hardened flies, suggesting that tropical populations have a greater hardening response. A similar pattern was evident for ramping heat knockdown time at 0.06 °C min^?1 increase. There was no cline for ramping heat knockdown temperature (CT_max) at 0.1 °C min^?1 increase. Acute (static) heat knockdown temperature increased towards temperate latitudes, probably reflecting a greater capacity of temperate flies to withstand sudden temperature increases during summer in temperate Australia. Larval viability showed a quadratic association with latitude under heat stress. Thus, patterns of heat resistance depend on assay methods. Genetic correlations in thermotolerance across life stages and evolutionary potential for critical thermal limits should be the focus of future studies.     

Increased body size confers greater fitness at lower experimental temperature in male Drosophila melanogaster

Genetic variation of body size along latitudinal clines is found globally in Drosophila melanogaster, with larger individuals encountered at higher latitudes. Temperature has been implicated as a selective agent for these clines, because the body size of laboratory populations allowed to evolve in culture at lower temperatures is larger. In this study, we investigated the hypothesis that larger size is favoured at lower temperature through natural selection on adult males. We measured life‐span and age‐specific fertility of males from lines of flies artificially selected for body size at two different experimental temperatures. There was an interaction between experimental temperature and body size selection for male fitness; large‐line males were fitter than controls at both temperatures, but the difference in fitness was greater at the lower experimental temperature. Smaller males did not perform significantly differently from control males at either experimental temperature. The results imply that thermal selection for larger adult males is at least in part responsible for the evolution of larger body size at lower temperatures in this species. The responsible mechanisms require further investigation.     

Clinal variation and laboratory adaptation in the rainforest species Drosophila birchii for stress resistance, wing size, wing shape and development time

Clinal variation has been described in many invertebrates including drosophilids but usually over broad geographical gradients. Here we describe clinal variation in the rainforest species Drosophila birchii from Queensland, Australia, and potential confounding effects of laboratory adaptation. Clinal variation was detected for starvation and development time, but not for size or resistance to temperature extremes. Starvation resistance was higher at southern locations. Wing shape components were not associated with latitude although they did differ among populations. Time in laboratory culture did not influence wing size or heat knockdown resistance, but increased starvation resistance and decreased recovery time following a cold shock. Laboratory culture also increased development time and altered wing shape. The results indicate that clinal patterns can be detected in Drosophila over a relatively narrow geographical area. Laboratory adaptation is unlikely to have confounded the detection of geographical patterns.     

Inferences of Demography and Selection in an African Population of Drosophila melanogaster

It remains a central problem in population genetics to infer the past action of natural selection, and these inferences pose a challenge because demographic events will also substantially affect patterns of polymorphism and divergence. Thus it is imperative to explicitly model the underlying demographic history of the population whenever making inferences about natural selection. In light of the considerable interest in adaptation in African populations of Drosophila melanogaster, which are considered ancestral to the species, we generated a large polymorphism data set representing 2.1 Mb from each of 20 individuals from a Ugandan population of D. melanogaster. In contrast to previous inferences of a simple population expansion in eastern Africa, our demographic modeling of this ancestral population reveals a strong signature of a population bottleneck followed by population expansion, which has significant implications for future demographic modeling of derived populations of this species. Taking this more complex underlying demographic history into account, we also estimate a mean X-linked region-wide rate of adaptation of 6 × 10⁻¹¹/site/generation and a mean selection coefficient of beneficial mutations of 0.0009. These inferences regarding the rate and strength of selection are largely consistent with most other estimates from D. melanogaster and indicate a relatively high rate of adaptation driven by weakly beneficial mutations.     

Autosomal variation for male body size and sperm competition phenotypes is uncorrelated in Drosophila melanogaster

Correlations between male body size and phenotypes impacting post-copulatory sexual selection are commonly observed during the manipulation of male body size by environmental rearing conditions. Here, we control for environmental influences and test for genetic correlations between natural variation in male body size and phenotypes affecting post-copulatory sexual selection in Drosophila melanogaster. Dry weights of virgin males from 90 second-chromosome and 88 third-chromosome substitution lines were measured. Highly significant line effects (p<0.001) documented a genetic basis to variation in male body size. No significant correlations were identified between male body size and the components of sperm competitive ability. These results suggest that natural autosomal variation for male body size has little impact on post-copulatory sexual selection. If genetic correlations exist between male body size and post-copulatory sexual selection then variation in the sex chromosomes are likely candidates, as might be expected if sexually antagonistic coevolution was responsible.     

Contrasting patterns of geographic variation in the cosmopolitan sibling species Drosophila melanogaster and Drosophila simulans

An electrophoretic study was carried out to compare the geographic pattern of genetic variation in Drosophila simulans with that of its sibling species, Drosophila melanogaster. An identical set of 32 gene-protein loci was studied in four geographically distant populations of D. simulans and two populations of D. melanogaster, all originating from Europe and Africa. The comparison yielded the following results: (1) tropical populations of D. simulans were, in terms of the number of unique alleles, average heterozygosity per locus, and percentage of loci polymorphic, more variable than conspecific-temperate populations; (2) some loci in both species showed interpopulation differences in allele frequencies that suggest latitudinal clines; and (3) temperate-tropical genetic differentiation between populations was much less in D. simulans than in D. melanogaster. Similar differences between these two species have previously been shown for chromosomal, quantitative, physiological, and middle-repetitive DNA variation. Estimates of N _m (number of migrants per generation) from the spatial distribution of rare alleles suggest that both species have similar levels of interpopulation gene flow. These observations lead us to propose two competing hypotheses: the low level of geographic differentiation in D. simulans is due to its evolutionarily recent worldwide colonization and, alternatively, D. simulans has a narrower niche than D. melanogaster. Geographic variation data on different genetic elements (e.g., mitochondrial DNA, two-dimensional proteins, etc.) are required before these hypotheses can be adequately tested.We thank the Natural Science and Engineering Research Council of Canada for financial support (Grant A0235 to R.S.S.).     

Genome scans of variation and adaptive change: extended analysis of a candidate locus close to the phantom gene region in Drosophila melanogaster

Nucleotide variation in populations originating from the recent range expansion of a species should reflect their adaptation to new habitats as well as their demographic history. A survey of nucleotide variation at 109 noncoding X-chromosome fragments in a European population of Drosophila melanogaster allowed identifying some candidates to have been recently affected by positive selection. Adaptive changes leave a spatial differential footprint that can be used to discriminate among candidates by extending their study to neighboring regions. Here, we surveyed variation at an approximately 190-kb region spanning a locus exhibiting a significantly skewed frequency spectrum. A stretch of approximately 12 kb with reduced variation was detected within a continuously sequenced region that included the focal fragment. Moreover, the regions flanking this stretch exhibited an excess of high-frequency derived variants. Application of maximum likelihood ratio and goodness-of-fit tests suggested that the pattern of variation detected at the studied region (at cytological bands 17C-17D) might have been shaped by a recent selective change, most probably at or around the phantom gene that encodes CYP306A1, a cytochrome P450 enzyme in the ecdysteroidogenic pathway.     

A major shift in Daphnia genetic structure after the first ice‐free winter in a German reservoir

1. Climate warming may cause disruption of trophic linkages in aquatic ecosystems and lead to changes in abundance and genetic structure of zooplankton populations. We monitored the community of the Daphnia galeata‐hyalina hybrid complex in the Saidenbach Reservoir (Saxony, Germany) using allozyme electrophoresis for three consecutive years (2005–07), including one (2007) following an unusually warm winter that prevented the formation of ice cover for the first time in the history of the reservoir. 2. Genetic composition during the 2007 season differed substantially from the two preceding years that experienced the usual 3‐month ice period. Three abundance peaks in June, July and October 2007 were dominated by hybrids of Daphnia galeata x hyalina, whereas in the 2005 and 2006 seasons two peaks in June and September were dominated by Daphnia hyalina genotypes. 3. The genetic composition of the pool of diapausing eggs produced in autumn and the rate of change of genotype abundance during the following spring indicate recruitment of the D. hyalina subpopulation from ex‐ephippial animals during the spring population increase. 4. The differing potential to contribute to the overwintering animal pool or to the inoculum from diapausing eggs was confirmed by results from laboratory life‐table experiments. Daphnia galeata clones survived longer and produced parthenogenetic offspring under winter conditions, whereas D. hyalina clones showed a shorter lifespan and produced resting eggs. 5. Our results indicate a profound role of recruitment strategy in the observed shift in genetic composition. Increasing winter temperatures predicted in the context of climate change may thus favour overwintering animals, leading to an increase in the contribution of these genotypes to the population. Such microevolutionary processes may dampen possible seasonal mismatches between daphnid populations and their food or predator populations.     

The genetics of dopa decarboxylase in Drosophila melanogaster. III. Effects of a temperature sensitive dopa decarboxylase deficient mutation on female fertility

The mutation Ddc^ts1 effects female sterility when homozygous, hemizygous, or heterozygous over a series of Ddc null alleles (Ddc^x) indicating that some aspect of Ddc gene function is necessary for female fertility. Ovary transplant experiments demonstrate that the female sterility phenotype is ovary autonomous. Two to 3% of the total DDC activity measurable in newly hatched females is localized in their previtellogenic ovaries. The degree to which females heterozygous for Ddc^ts1 over different Ddc null alleles are fertile at 22°C reflects a continuous spectrum of allelic complementation similar to that observed for the effects of these genotypes on viability at 30°C. Fertility of all the Ddc^ts1/Ddc^x females tested is significantly depressed at 30 vis-a-vis 22°C providing evidence that it is the DDC enzyme activity itself which is required for female fertility. Ddc^ts1/Ddc^ts1 homozygous and Ddc^ts1/Df hemizygous females are nonconditionally, completely sterile at 18, 20, 22, 25, and 30°C. Although all homo- and hemizygous females do lay some eggs, no evidence of embryogenesis or fertilization has ever been detected. The absolute, nonconditional sterility of Ddc^ts1 homo- and hemizygous females stands in stark contrast to the conventional temperature dependent effects of these same genotypes on viability and to the temperature sensitive effects of Ddc^ts1/Ddc^x heterozygous females on both fertility and viability. Reasons for these tissue-specific and genotypic differences are discussed.     

Drosophila mojoless, a retroposed GSK-3, has functionally diverged to acquire an essential role in male fertility

Retroposition is increasingly recognized as an important mechanism for the acquisition of new genes. We show that a glycogen synthase kinase-3 gene, shaggy (sgg), retroposed at least 50 MYA in the Drosophila genus to generate a new gene, mojoless (mjl). We have extensively analyzed the function of mjl and examined its functional divergence from the parental gene sgg in Drosophila melanogaster. Unlike Sgg, which is expressed in many tissues of both sexes, Mjl is expressed specifically in the male germ line, where it is required for male germ line survival. Our analysis indicates that mjl has acquired a specific function in the maintenance of male germ line viability. However, it has not completely lost its ancestral biochemical function and can partially compensate for loss of the parental gene sgg when ectopically expressed in somatic cells. We postulate that mjl has undergone functional diversification and is now under stabilizing selection in the Drosophila genus.     

Longevity and resistance to cold stress in cold‐stress selected lines and their controls in Drosophila melanogaster

Thermal environments can influence many fitness‐related traits including life span. Here, we assess whether longevity in Drosophila melanogaster can experimentally evolve as a correlated response to cold‐stress selection, and whether genotype‐by‐temperature and sex‐by‐temperature interactions are significant components of variation in life span. Three replicated S lines were cold‐stress selected and compared with their respective unselected controls (Clines) in the 16^th generation of thermal selection. Cold‐stress resistance exhibited a substantial direct response to selection, and also showed a significant interaction between sex and type of line. Mean longevity exhibited a significant interaction between adult test temperature (14 and 25 °C) and line (with suggestive evidence for increased longevity of S lines when tested at 14 °C), but there was no evidence for increased longevity in S lines at normal temperatures (i.e. 25 °C). Another temperature‐dependent effect was sex‐specific, with males being the longer lived sex at 25 °C but the less long‐lived sex at 14 °C. Additionally, we tested in an exploratory way the relationship between longevity and cold‐stress resistance by also measuring resistance to a prefreezing temperature before and after one generation of longevity selection at 14 °C (selection intensity, i = 1.47 for S lines, and 1.42 for C lines). In this longevity selection, we found that cold‐stress resistance increased by about 6% in S lines and 18% in C lines. However, taken together, the results indicate no simple relationship between longevity and cold‐stress resistance, with genotype‐by‐sex interactions in both traits. Temperature dependent interaction in longevity is apparent between S and C lines, and sex‐specific variation in mean longevity also depends on temperature.     

Climate change,boundary increase and elongation of a pre‐existing cline: A case study in Drosophila ananassae

During the past two to three decades, Drosophila ananassae, a warm adapted tropical species, has invaded low to mid altitude localities in the western Himalayas. Due to its cold sensitivity, this species had never been recorded from higher latitudes as well as altitudes in India to the 1960s. A latitudinal cline in this desiccation‐sensitive species corresponds with southern humid tropical localities rather than northern drier subtropical localities. An extension of its cline into lowland to midland montane localities has resulted due to global climatic change as well as local thermal effects through anthropogenic impact. However, D. ananassae populations at species borders are characterized by lower genetic variability for body melanization as well as for desiccation resistance. There is a lack of thermal plastic effects for body melanization, and the observed extended cline might represent evolutionary (genetic) response due to selection pressure imposed by drier habitats. A comparison of fecundity, hatchability and viability at three growth temperatures (17, 20 and 25°C) showed significant reduction in trait values at 17°C in D. ananassae. Thus, its recent range expansion into northern montane localities might involve genetic effects on stress‐related traits and plastic effects on life history traits. We suggest that D. ananassae could serve as an indicator species for analyzing range expansion under changing climatic conditions.     

Climate effects on inter‐annual variation in growth of the freshwater mussel (Anodonta beringiana) in an Alaskan lake

1. Warming trends are evident in many parts of the globe but are especially marked at higher latitudes, with complex effects on the biota that include direct effects on growth potential and indirect effects through food webs. 2. Air temperatures have been increasing over the past 50 years in southwestern Alaska, affecting the growth and population dynamics of many organisms, including a variety of aquatic species such as the freshwater mussel Anodonta beringiana. 3. We collected freshwater mussels from Iliamna Lake, in the Bristol Bay region of Alaska, and measured their shells to examine climatic effects on growth patterns. 4. Linear mixed effects models and ordinary least square linear regressions revealed strong positive correlations between local air temperatures (especially in May, October and the summer months) and inter‐annual variation in mussel growth. Slower mussel growth was also significantly correlated with later date of ice break‐up, which was linked to air temperatures in late spring.     

The effect of fire and permafrost interactions on soil carbon accumulation in an upland black spruce ecosystem of interior Alaska: implications for post‐thaw carbon loss

High‐latitude regions store large amounts of organic carbon (OC) in active‐layer soils and permafrost, accounting for nearly half of the global belowground OC pool. In the boreal region, recent warming has promoted changes in the fire regime, which may exacerbate rates of permafrost thaw and alter soil OC dynamics in both organic and mineral soil. We examined how interactions between fire and permafrost govern rates of soil OC accumulation in organic horizons, mineral soil of the active layer, and near‐surface permafrost in a black spruce ecosystem of interior Alaska. To estimate OC accumulation rates, we used chronosequence, radiocarbon, and modeling approaches. We also developed a simple model to track long‐term changes in soil OC stocks over past fire cycles and to evaluate the response of OC stocks to future changes in the fire regime. Our chronosequence and radiocarbon data indicate that OC turnover varies with soil depth, with fastest turnover occurring in shallow organic horizons (～60 years) and slowest turnover in near‐surface permafrost (>3000 years). Modeling analysis indicates that OC accumulation in organic horizons was strongly governed by carbon losses via combustion and burial of charred remains in deep organic horizons. OC accumulation in mineral soil was influenced by active layer depth, which determined the proportion of mineral OC in a thawed or frozen state and thus, determined loss rates via decomposition. Our model results suggest that future changes in fire regime will result in substantial reductions in OC stocks, largely from the deep organic horizon. Additional OC losses will result from fire‐induced thawing of near‐surface permafrost. From these findings, we conclude that the vulnerability of deep OC stocks to future warming is closely linked to the sensitivity of permafrost to wildfire disturbance.