Distribution modelling of an introduced species: do adaptive genetic markers affect potential range?

Biological invasions have increased in the last few decades mostly due to anthropogenic causes such as globalization of trade. Because invaders sometimes cause large economic losses and ecological disturbances, estimating their origin and potential geographical ranges is useful. Drosophila subobscura is native to the Old World but was introduced in the New World in the late 1970s and spread widely. We incorporate information on adaptive genetic markers into ecological niche modelling and then estimate the most probable geographical source of colonizers; evaluate whether the genetic bottleneck experienced by founders affects their potential distribution; and finally test whether this species has spread to all its potential suitable habitats worldwide. We find the environmental space occupied by this species in its native and introduced distributions are notably the same, although the introduced niche has shifted slightly towards higher temperature and lower precipitation. The genetic bottleneck of founding individuals was a key factor limiting the spread of this introduced species. We also find that regions in the Mediterranean and north-central Portugal show the highest probability of being the origin of the colonizers. Using genetically informed environmental niche modelling can enhance our understanding of the initial colonization and spread of invasive species, and also elucidate potential areas of future expansions worldwide.

Evolutionary principles and their practical application.

Evolutionary principles are now routinely incorporated into medicine and agriculture. Examples include the design of treatments that slow the evolution of resistance by weeds, pests, and pathogens, and the design of breeding programs that maximize crop yield or quality. Evolutionary principles are also increasingly incorporated into conservation biology, natural resource management, and environmental science. Examples include the protection of small and isolated populations from inbreeding depression, the identification of key traits involved in adaptation to climate change, the design of harvesting regimes that minimize unwanted life-history evolution, and the setting of conservation priorities based on populations, species, or communities that harbor the greatest evolutionary diversity and potential. The adoption of evolutionary principles has proceeded somewhat independently in these different fields, even though the underlying fundamental concepts are the same. We explore these fundamental concepts under four main themes: variation, selection, connectivity, and eco-evolutionary dynamics. Within each theme, we present several key evolutionary principles and illustrate their use in addressing applied problems. We hope that the resulting primer of evolutionary concepts and their practical utility helps to advance a unified multidisciplinary field of applied evolutionary biology.

Three selections are better than one: clinal variation of thermal QTL from independent selection experiments in Drosophila.

We report the results of two independent selection experiments that have exposed distinct populations of Drosophila melanogaster to different forms of thermal selection. A recombinant population derived from Arvin California and Zimbabwe isofemale lines was exposed to laboratory natural selection at two temperatures (T(AZ): 18°C and 28°C). Microsatellite mapping identified quantitative trait loci (QTL) on the X-chromosome between the replicate "Hot" and "Cold" populations. In a separate experiment, disruptive selection was imposed on an outbred California population for the "knockdown" temperature (T(KD)) in a thermal column. Microsatellite mapping of the "High" and "Low" populations also uncovered primarily X-linked QTL. Notably, a marker in the shaggy locus at band 3A was significantly differentiated in both experiments. Finer scale mapping of the 3A region has narrowed the QTL to the shaggy gene region, which contains several candidate genes that function in circadian rhythms. The same allele that was increased in frequency in the High T(KD) populations is significantly clinal in North America and is more common at the warm end of the cline (Florida vs. Maine; however, the cline was not apparent in Australia). Together, these studies show that independent selection experiments can uncover the same target of selection and that evolution in the laboratory can recapitulate putatively adaptive clinal variation in nature.

A framework for community interactions under climate change.

Predicting the impacts of climate change on species is one of the biggest challenges that ecologists face. Predictions routinely focus on the direct effects of climate change on individual species, yet interactions between species can strongly influence how climate change affects organisms at every scale by altering their individual fitness, geographic ranges and the structure and dynamics of their community. Failure to incorporate these interactions limits the ability to predict responses of species to climate change. We propose a framework based on ideas from global-change biology, community ecology, and invasion biology that uses community modules to assess how species interactions shape responses to climate change.

A contemporary, sex-limited change in body size of an estuarine turtle in response to commercial fishing.

Juvenile growth rate and adult body size are important components of life-history strategies because of their direct impact on fitness. The diamondback terrapin (Malaclemys terrapin) is a sexually dimorphic, long-lived turtle inhabiting brackish waters throughout the Atlantic and Gulf coasts of the United States. In parts of its range, terrapins face anthropogenically imposed mortality: juveniles of both sexes inadvertently enter commercial crab traps and drown. For adult females, the carapace eventually grows large enough that they cannot enter traps, whereas males almost never reach that critical size. We compared age structure, carapace dimensions, growth curves, and indices of sexual dimorphism for a Chesapeake Bay population of terrapins (where mortality of turtles is high due to crab traps) with contemporary terrapins from Long Island Sound and museum specimens from Chesapeake Bay (neither group subject to commercial crab traps). We also calculated the allochronic and synchronic rates of evolutionary change (haldanes) for males and females to measure the rate of trait change in a population or between populations, respectively. We found a dramatic shift to a younger male age structure, a decrease in the length of time to terminal female carapace size, a 15% increase in female carapace width, and an increase in sexual dimorphism in Chesapeake Bay. In a new twist, our results implicate a fishery in the selective increase in size of a reptilian bycatch species. These sex-specific changes in life history and demography have implications for population viability that need to be considered when addressing conservation of this threatened turtle.

Underutilized resources for studying the evolution of invasive species during their introduction, establishment, and lag phases.

The early phases of biological invasions are poorly understood. In particular, during the introduction, establishment, and possible lag phases, it is unclear to what extent evolution must take place for an introduced species to transition from established to expanding. In this study, we highlight three disparate data sources that can provide insights into evolutionary processes associated with invasion success: biological control organisms, horticultural introductions, and natural history collections. All three data sources potentially provide introduction dates, information about source populations, and genetic and morphological samples at different time points along the invasion trajectory that can be used to investigate preadaptation and evolution during the invasion process, including immediately after introduction and before invasive expansion. For all three data sources, we explore where the data are held, their quality, and their accessibility. We argue that these sources could find widespread use with a few additional pieces of data, such as voucher specimens collected at certain critical time points during biocontrol agent quarantine, rearing, and release and also for horticultural imports, neither of which are currently done consistently. In addition, public access to collected information must become available on centralized databases to increase its utility in ecological and evolutionary research.

Evolution of Chilean colonizing populations of Drosophila subobscura: lethal genes and chromosomal arrangements.

Knowledge of the frequency, distribution, and fate of lethal genes in chromosomal inversions helps to illuminate the evolution of recently founded populations. We analyze the relationship between lethal genes and inversions in two colonizing populations of D. subobscura in Chile. In the ancestral Palearctic populations of this species, lethal genes seem distributed at random on chromosomes. But in colonizing American populations, some lethal genes are associated with specific chromosomal arrangements. Some of these associated lethals were detected only during the first stages of the colonization (O( 3+4+2 )), and never thereafter, whereas others have persisted (O( 3+4+7 ) and O(5)). However, most lethal genes in American populations have been observed only once: they have arisen by novel mutation and soon disappear. Finally, recombination between different inversions has been observed in America. However, the persistence of lethal genes associated with the heterotic inversions O( 3+4+7 ) and O(5) could indicate that recombination inside these inversions is rare.

Correction of statistical miscalculation slightly alters conclusions about diversity effects for Douglass et al. (2008).

While most of the conclusions about diversity effects in Douglass, J.G., Duffy, J.E. & Bruno, J.F. [Ecol. Lett., 11, 2008, 1] are upheld, correction of a statistical miscalculation indicates that grazer diversity and predator diversity had combined effects on responses, but did not have interactive effects as initially reported.

Clinal patterns of desiccation and starvation resistance in ancestral and invading populations of Drosophila subobscura.

As invading species expand, they eventually encounter physical and biotic stressors that limit their spread. We examine latitudinal and climatic variation in physiological tolerance in one native and two invading populations of Drosophila subobscura. These flies are native to the Palearctic region, but invaded both South and North America around 1980 and spread rapidly across 15° of latitude on each continent. Invading flies rapidly evolved latitudinal clines in chromosome inversion frequencies and in wing size that parallel those of native populations in the Old World. Here we investigate whether flies on all three continents have evolved parallel clines in desiccation and starvation tolerance, such that flies in low-latitude regions (hot, dry) might have increased stress resistance. Starvation tolerance does not vary with latitude or climate on any continent. In contrast, desiccation tolerance varies clinally with latitude on all three continents, although not in parallel. In North American and Europe, desiccation tolerance is inversely related to latitude, as expected. But in South America, desiccation tolerance increases with latitude and is greatest in relatively cool and wet areas. Differences among continents in latitudinal patterns of interspecific-competition potentially influence clinal selection for physiological resistance, but no simple pattern is evident on these continents.

Critical thermal maxima in knockdown-selected Drosophila: are thermal endpoints correlated?

To explore the correlation of traits linked to thermotolerance, we compared three thermal endpoints (knockdown temperature and two critical thermal maxima) among replicate populations of Drosophila melanogaster selected for high, or low, knockdown temperature. The high knockdown flies maintain normal posture and locomotor ability within a knockdown column at temperatures >or=40 degrees C, whereas the low knockdown flies fall out of the column at much cooler temperatures (approximately 35 degrees C, on average). The critical thermal maximum (CT(max)) for respiratory control in the selected knockdown populations was determined by analyzing CO(2) output of individuals during exposure to a temperature ramp (from 30 degrees C to >45 degrees C) and was indicated by an abrupt alteration in the pattern of CO(2) release. The CT(max) for locomotor function was determined by monitoring activity (concurrent with CO(2) analysis) during the temperature ramp and was marked by the abrupt cessation of activity. We hypothesized that selection for high knockdown temperature may cause an upward shift in CT(max), whereas selection for low knockdown may lower CT(max). Correlations among the three thermal endpoints varied between the high and low knockdown flies. Finally, we compared metabolic profiles, as well as Q(10) values, among the high and low knockdown males and females during the temperature ramp.

All stressed out and nowhere to go: does evolvability limit adaptation in invasive species? An introduction to the symposium at the SSE/ASN/SSB meeting, June 2004.

Introduced and invasive species are major threats native species and communities and, quite naturally, most scientists and managers think of them in terms of ecological problems. However, species introductions are also experiments in evolution, both for the alien species and for the community that they colonize. We focus here on the introduced species because these offer opportunities to study the properties that allow a species to succeed in a novel habitat and the constraints that limit range expansion. Moreover, an increasing body of evidence from diverse taxa suggests that the introduced species often undergo rapid and observable evolutionary change in their new habitat. Evolution requires genetic variation, which may be decreased or expanded during an invasion, and an evolutionary mechanism such as genetic drift or natural selection. In this volume, we seek to understand how natural selection produces adaptive evolution during invasions. Key questions include what is the role of biotic and abiotic stress in driving adaptation, and what is the source of genetic variation in introduced populations.

Selection on knockdown performance in Drosophila melanogaster impacts thermotolerance and heat-shock response differently in females and males.

We studied adaptive thermotolerance in replicate populations of Drosophila melanogaster artificially selected for high and low knockdown temperature (T(KD)), the upper temperature at which flies can no longer remain upright or locomote effectively. Responses to selection have generated High T(KD) populations capable of maintaining locomotor function at approximately 40 degrees C, and Low T(KD) populations with T(KD) of approximately 35 degrees C. We examined inducible knockdown thermotolerance, as well as inducible thermal survivorship, following a pretreatment heat-shock (known to induce heat-shock proteins) for males and females from the T(KD) selected lines. Both selection for knockdown and sex influenced inducible knockdown thermotolerance, whereas inducible thermal survivorship was influenced only by sex, and not by selection. Overall, our findings suggest that the relationships between basal and inducible thermotolerance are contingent upon the methods used to gauge thermotolerance, as well as the sex of the flies. Finally, we compared temporal profiles of the combined expression of two major heat-shock proteins, HSC70 and HSP70, during heat stress among the females and males from the selected T(KD) lines. The temporal profiles of the proteins differed between High and Low T(KD) females, suggesting divergence of the heat-shock response. We discuss a possible mechanism that may lead to the heat-shock protein patterns observed in the selected females.

Global genetic change tracks global climate warming in Drosophila subobscura.

Comparisons of recent with historical samples of chromosome inversion frequencies provide opportunities to determine whether genetic change is tracking climate change in natural populations. We determined the magnitude and direction of shifts over time (24 years between samples on average) in chromosome inversion frequencies and in ambient temperature for populations of the fly Drosophila subobscura on three continents. In 22 of 26 populations, climates warmed over the intervals, and genotypes characteristic of low latitudes (warm climates) increased in frequency in 21 of those 22 populations. Thus, genetic change in this fly is tracking climate warming and is doing so globally.

Sexual size dimorphism in a Drosophila clade, the D. obscura group.

The Drosophila obscura clade consists of about 41 species, of which 20 were used for analyses of wing and thorax length. Our primary goal was to investigate the magnitude of sexual size dimorphism (SSD) of these traits within this clade and to test Rensch's Rule [when females are larger than males, SSD (e.g., female/male ratio) should decrease with body size]. Our secondary goal was methodological and involved evaluating for these flies alternative measures of SSD (female/male ratio, female/male absolute difference, female/male relative difference), developing a bootstrap method to estimate the magnitude of intraspecific variation in SSD, and applying a new method of estimating allometric relationships that is phylogenetically based and incorporates error variance in both traits. All indices of SSD were strongly correlated for both size traits. Nevertheless, female/male ratio is the best index here: it is easily interpretable and essentially independent of size. For both traits, SSD (F/M) varied interspecifically, showed a strong phylogenetic signal, but did not differ for the main phylogenetic subgroups or correlate with latitude. Factors underlying variation in SSD in this clade are elusive and might include genetic drift. SSD (wing) tended to decrease with increasing size, as predicted by Rensch's Rule, though not consistently so. SSD (thorax) was unrelated to size. However, analysis of published data for thorax length of Drosophila spp. (N=42) with a larger size range showed that SSD decreased significantly with increasing size (consistent with Rensch's Rule), suggesting our ability to detect SSD-size relations in the D. obscura data may be limited by low statistical power.

A time series of evolution in action: a latitudinal cline in wing size in South American Drosophila subobscura.

Drosophila subobscura is geographically widespread in the Old World. Around the late 1970s, it was accidentally introduced into both South and North America, where it spread rapidly over broad latitudinal ranges. This invading species offers opportunities to study the speed and predictability of trait evolution on a geographic scale. One trait of special interest is body size, which shows a strong and positive latitudinal cline in many Drosophila species, including Old World D. subobscura. Surveys made about a decade after the invasion found no evidence of a size cline in either North or South America. However, a survey made in North America about two decades after the invasion showed that a conspicuous size cline had evolved and (for females) was coincident with that for Old World flies. We have now conducted parallel studies on 10 populations (13 degrees of latitude) of flies, collected in Chile in spring 1999. After rearing flies in the laboratory for several generations, we measured wing sizes and compared geographic patterns (versus latitude or temperature) for flies on all three continents. South American females have now evolved a significant latitudinal size cline that is similar in slope to that of Old World and of North American flies. Rates of evolution (haldanes) for females are among the highest ever measured for quantitative traits. In contrast, the size cline is positive but not significant for South or North American males. At any given latitude, South American flies of both sexes are relatively large; this in part reflects the relatively cool climate of coastal Chile. Interestingly, the sections of the wing that generate the size cline for females differ among all three continents. Thus, although the evolution of overall wing size is predictable on a geographic scale (at least for females), the evolution of size of particular wing components is decidedly not.

Plastic and Genetic Variation in Wing Loading as a Function of Temperature Within and Among Parallel Clines in Drosophila subobscura.

Drosophila subobscura is a European (EU) species that was introduced into South America (SA) approximately 25 years ago. Previous studies have found rapid clinal evolution in wing size and in chromosome inversion frequency in the SA colonists, and these clines parallel those found among the ancestral EU populations. Here we examine thermoplastic changes in wing length in flies reared at 15, 20, and 25°C from 10 populations on each continent. Wings are plastically largest in flies reared at 15°C (the coldest temperature) and genetically largest from populations that experience cooler temperatures on both continents. We hypothesize that flies living in cold temperatures benefit from reduced wing loading: ectotherms with cold muscles generate less power per wing beat, and hence larger wings and/or a smaller mass would facilitate fight. We develop a simple null model, based on isometric growth, to test our hypothesis. We find that both EU and SA flies exhibit adaptive plasticity in wing loading: flies reared at 15°C generally have lower wing loadings than do flies reared at 20°C or 25°C. Clinal patterns, however, are strikingly different. The ancestral EU populations show adaptive clinal variation at rearing a temperature of 15°C: flies from cool climates have lower wing loadings. In the colonizing populations from SA, however, we cannot reject the null model: wing loading increases with decreasing clinal temperatures. Our data suggest that selective factors other than flight have favored the rapid evolution of large overall size at low environmental temperatures. However, selection for increased flight ability in such environments may secondarily favor reduced body mass.

Evolutionary pace of chromosomal polymorphism in colonizing populations of Drosophila subobscura: an evolutionary time series.

Biologists have long debated the speed, uniformity, and predictability of evolutionary change. However, evaluating such patterns on a geographic scale requires time-series data on replicate sets of natural populations. Drosophila subobscura has proven an ideal model system for such studies. This fly is broadly distributed in the Old World, but was introduced into both North and South America just over two decades ago and then spread rapidly. Rapid, uniform, and predictable evolution would be demonstrated if the invading flies evolved latitudinal clines that progressively converged on those of the native populations. Evolutionary geneticists quickly capitalized on this opportunity to monitor evolutionary dynamics. Just a few years after the introduction, they surveyed chromosomal inversion frequencies in both North and South America. On both continents they detected incipient latitudinal clines in chromosome inversion frequencies that almost always had the same sign with latitude as in the Old World. Thus the initial evolution of chromosomal polymorphisms on a continental scale was remarkably rapid and consistent. Here we report newer samples of inversion frequencies for the colonizing populations: the time series now spans almost one decade for North America and almost two decades for South America. Almost all inversions in the New World continue to show the same sign of frequency with latitude as in the Old World. Nevertheless, inversion clines have not consistently increased in steepness over time; nor have they consistently continued to converge on the Old World baseline. However, five arrangements in South America show directional, continentwide shifts in frequency. Overall, the initial consistency of clinal evolutionary trajectories seen in the first surveys seems not to have been maintained.

Different cell size and cell number contribution in two newly established and one ancient body size cline of Drosophila subobscura.

Latitudinal genetic clines in body size occur in many ectotherms including Drosophila species. In the wing of D. melanogaster, these clines are generally based on latitudinal variation in cell number. In contrast, differences in wing area that evolve by thermal selection in the laboratory are in general based on cell size. To investigate possible reasons for the different cellular bases of these two types of evolutionary response, we compared the newly established North and South American wing size clines of Drosophila subobscura. The new clines are based on latitudinal variation in cell area in North America and cell number in South America. The ancestral European cline is also based on latitudinal variation in cell number. The difference in the cellular basis of wing size variation in the American clines, which are roughly the same age, together with the similar cellular basis of the new South American cline and the ancient European one, suggest that the antiquity of a cline does not explain its cellular basis. Furthermore, the results indicate that wing size as a whole, rather than its cellular basis, is under selection. The different cellular bases of different size clines are most likely explained either entirely by chance or by different patterns of genetic variance--or its expression--in founding populations.

Mutation accumulation, performance, fitness.

The morphology-performance-fitness paradigm is usually explored by determining whether natural or "phenotypically engineered" variation among individuals in morphology (physiology) or performance covaries with an index of fitness such as survival. Here we study between-line covariation between performance and fitness for 44 lines of flies that had undergone mutation accumulation (in the absence of natural selection) on the second chromosome for 62 generations, plus 13 control lines. These mutation accumulation (MA) lines were known to have reduced competitive fitness and life history scores, and to have positive between-line covariances among life history traits. We measured several performance traits of larvae and adults (and a life history trait), examined covariances among those trait means, and also examined covariances of traits with competitive fitness. MA lines had significantly lower performances than did control lines in most traits. However, because control lines had been unknowingly contaminated, a conclusion that MA reduces performance must be tentative. Correlations among performance traits were highly variable in sign, suggesting that MA does not negatively affect all traits equivalently. Even so, correlation matrices for MA and for control lines were very similar. In bivariate comparisons, only one performance trait (a "get-a-grip index," which measures the ability of a falling fly to catch itself on baffles) was positively correlated with competitive fitness. Multivariate analyses again suggested the importance primarily of get-a-grip. Two main patterns emerge from this study. First, MA negatively affects diverse aspects of physiological performance, but does so differentially across traits. Second, except for GAG, MA-induced variation in performance is at best weakly correlated with competitive fitness.

WITHIN- AND BETWEEN-GENERATION EFFECTS OF TEMPERATURE ON THE MORPHOLOGY AND PHYSIOLOGY OF DROSOPHILA MELANOGASTER.

We investigated the effects of developmental and parental temperatures on several physiological and morphological traits of adult Drosophila melanogaster. Flies for the parental generation were raised at either low or moderate temperature (18°C or 25°C) and then mated in the four possible sex-by-parental temperature crosses. Their offspring were raised at either 18°C or 25°C and then scored as adults for morphological (dry body mass, wing size, and abdominal melanization [females only]), physiological (knock-down temperature, and thermal dependence of walking speed), and life history (egg size) traits. The experiment was replicated, and the factorial design allows us to determine whether and how paternal, maternal, and developmental temperatures (as well as offspring sex) influence the various traits. Sex and developmental temperature had major effects on all traits. Females had larger bodies and wings, higher knock-down temperatures, and slower speeds (but similar shaped performance curves) than males. Development at 25°C (versus at 18°C) increased knock-down temperature, increased maximal speed and thermal performance breadth, decreased the optimal temperature for walking, decreased body mass and wing size, reduced abdominal melanization, and reduced egg size. Parental temperatures influenced a few traits, but the effects were generally small relative to those of sex or developmental temperature. Flies whose mother had been raised at 25°C (versus at 18°C) had slightly higher knock-down temperature and smaller body mass. Flies whose father had been raised at 25°C had relatively longer wings. The effects of paternal, maternal, and developmental temperatures sometimes differed in direction. The existence of significant within- and between-generation effects suggests that comparative studies need to standardize thermal environments for at least two generations, that attempts to estimate "field" heritabilities may be unreliable for some traits, and that predictions of short-term evolutionary responses to selection will be difficult.