Seasonal variation in life history traits in two Drosophila species

Seasonal environmental heterogeneity is cyclic, persistent and geographically widespread. In species that reproduce multiple times annually, environmental changes across seasonal time may create different selection regimes that may shape the population ecology and life history adaptation in these species. Here, we investigate how two closely related species of Drosophila in a temperate orchard respond to environmental changes across seasonal time. Natural populations of Drosophila melanogaster and Drosophila simulans were sampled at four timepoints from June through November to assess seasonal change in fundamental aspects of population dynamics as well as life history traits. D. melanogaster exhibit pronounced change across seasonal time: early in the season, the population is inferred to be uniformly young and potentially represents the early generation following overwintering survivorship. D. melanogaster isofemale lines derived from the early population and reared in a common garden are characterized by high tolerance to a variety of stressors as well as a fast rate of development in the laboratory environment that declines across seasonal time. In contrast, wild D. simulans populations were inferred to be consistently heterogeneous in age distribution across seasonal collections; only starvation tolerance changed predictably over seasonal time in a parallel manner as in D. melanogaster. These results suggest fundamental differences in population and evolutionary dynamics between these two taxa associated with seasonal heterogeneity in environmental parameters and associated selection pressures.     

The microbiota influences the Drosophila melanogaster life history strategy

Organisms are locally adapted when members of a population have a fitness advantage in one location relative to conspecifics in other geographies. For example, across latitudinal gradients, some organisms may trade off between traits that maximize fitness components in one, but not both, of somatic maintenance or reproductive output. Latitudinal gradients in life history strategies are traditionally attributed to environmental selection on an animal's genotype, without any consideration of the possible impact of associated microorganisms (“microbiota”) on life history traits. Here, we show in Drosophila melanogaster, a key model for studying local adaptation and life history strategy, that excluding the microbiota from definitions of local adaptation is a major shortfall. First, we reveal that an isogenic fly line reared with different bacteria varies the investment in early reproduction versus somatic maintenance. Next, we show that in wild fruit flies, the abundance of these same bacteria was correlated with the latitude and life history strategy of the flies, suggesting geographic specificity of the microbiota composition. Variation in microbiota composition of locally adapted D. melanogaster could be attributed to both the wild environment and host genetic selection. Finally, by eliminating or manipulating the microbiota of fly lines collected across a latitudinal gradient, we reveal that host genotype contributes to latitude‐specific life history traits independent of the microbiota and that variation in the microbiota can suppress or reverse the differences between locally adapted fly lines. Together, these findings establish the microbiota composition of a model animal as an essential consideration in local adaptation.     

Life history evolution and cellular mechanisms associated with increased size in high‐altitude Drosophila

Understanding the physiological and genetic basis of growth and body size variation has wide‐ranging implications, from cancer and metabolic disease to the genetics of complex traits. We examined the evolution of body and wing size in high‐altitude Drosophila melanogaster from Ethiopia, flies with larger size than any previously known population. Specifically, we sought to identify life history characteristics and cellular mechanisms that may have facilitated size evolution. We found that the large‐bodied Ethiopian flies laid significantly fewer but larger eggs relative to lowland, smaller‐bodied Zambian flies. The highland flies were found to achieve larger size in a similar developmental period, potentially aided by a reproductive strategy favoring greater provisioning of fewer offspring. At the cellular level, cell proliferation was a strong contributor to wing size evolution, but both thorax and wing size increases involved important changes in cell size. Nuclear size measurements were consistent with elevated somatic ploidy as an important mechanism of body size evolution. We discuss the significance of these results for the genetic basis of evolutionary changes in body and wing size in Ethiopian D. melanogaster.     

Variation in chronic radiation exposure does not drive life history divergence among Daphnia populations across the Chernobyl Exclusion Zone

Ionizing radiation is a mutagen with known negative impacts on individual fitness. However, much less is known about how these individual fitness effects translate into population‐level variation in natural environments that have experienced varying levels of radiation exposure. In this study, we sampled genotypes of the freshwater crustacean, Daphnia pulex, from the eight inhabited lakes across the Chernobyl Exclusion Zone (CEZ). Each lake has experienced very different levels of chronic radiation exposure since a nuclear power reactor exploded there over thirty years ago. The sampled Daphnia genotypes represent genetic snapshots of current populations and allowed us to examine fitness‐related traits under controlled laboratory conditions at UK background dose rates. We found that whilst there was variation in survival and schedules of reproduction among populations, there was no compelling evidence that this was driven by variation in exposure to radiation. Previous studies have shown that controlled exposure to radiation at dose rates included in the range measured in the current study reduce survival, or fecundity, or both. One limitation of this study is the lack of available sites at high dose rates, and future work could test life history variation in various organisms at other high radiation areas. Our results are nevertheless consistent with the idea that other ecological factors, for example competition, predation or parasitism, are likely to play a much bigger role in driving variation among populations than exposure to the high radiation dose rates found in the CEZ. These findings clearly demonstrate that it is important to examine the potential negative effects of radiation across wild populations that are subject to many and varied selection pressures as a result of complex ecological interactions.     

The effect of gut microbiota elimination in Drosophila melanogaster: A how‐to guide for host–microbiota studies

In recent years, there has been a surge in interest in the effects of the microbiota on the host. Increasingly, we are coming to understand the importance of the gut microbiota in modulating host physiology, ecology, behavior, and evolution. One method utilized to evaluate the effect of the microbiota is to suppress or eliminate it, and compare the effect on the host with that of untreated individuals. In this study, we evaluate some of these commonly used methods in the model organism, Drosophila melanogaster. We test the efficacy of a low‐dose streptomycin diet, egg dechorionation, and an axenic or sterile diet, in the removal of gut bacteria within this species in a fully factorial design. We further determine potential side effects of these methods on host physiology by performing a series of standard physiological assays. Our results showed that individuals from all treatments took significantly longer to develop, and weighed less, compared to normal flies. Males and females that had undergone egg dechorionation weighed significantly less than streptomycin reared individuals. Similarly, axenic female flies, but not males, were much less active when analyzed in a locomotion assay. All methods decreased the egg to adult survival, with egg dechorionation inducing significantly higher mortality. We conclude that low‐dose streptomycin added to the dietary media is more effective at removing the gut bacteria than egg dechorionation and has somewhat less detrimental effects to host physiology. More importantly, this method is the most practical and reliable for use in behavioral research. Our study raises the important issue that the efficacy of and impacts on the host of these methods require investigation in a case‐by‐case manner, rather than assuming homogeneity across species and laboratories.     

Divergence of gastropod life history in contrasting thermal environments in a geothermal lake

Experiments using natural populations have provided mixed support for thermal adaptation models, probably because the conditions are often confounded with additional environmental factors like seasonality. The contrasting geothermal environments within Lake Mývatn, northern Iceland, provide a unique opportunity to evaluate thermal adaptation models using closely located natural populations. We conducted laboratory common garden and field reciprocal transplant experiments to investigate how thermal origin influences the life history of Radix balthica snails originating from stable cold (6 °C), stable warm (23 °C) thermal environments or from areas with seasonal temperature variation. Supporting thermal optimality models, warm‐origin snails survived poorly at 6 °C in the common garden experiment and better than cold‐origin and seasonal‐origin snails in the warm habitat in the reciprocal transplant experiment. Contrary to thermal adaptation models, growth rate in both experiments was highest in the warm populations irrespective of temperature, indicating cogradient variation. The optimal temperatures for growth and reproduction were similar irrespective of origin, but cold‐origin snails always had the lowest performance, and seasonal‐origin snails often performed at an intermediate level compared to snails originating in either stable environment. Our results indicate that central life‐history traits can differ in their mode of evolution, with survival following the predictions of thermal optimality models, whereas ecological constraints have shaped the evolution of growth rates in local populations.     

Experimental migration upward in elevation is associated with strong selection on life history traits

One of the strongest biological impacts of climate change has been the movement of species poleward and upward in elevation. Yet, what is not clear is the extent to which the spatial distribution of locally adapted lineages and ecologically important traits may also shift with continued climate change. Here, we take advantage of a transplant experiment mimicking up‐slope seed dispersal for a suite of ecologically diverse populations of yellow monkeyflower (Mimulus guttatus sensu lato) into a high‐elevation common garden during an extreme drought period in the Sierra Nevada mountains, California, USA. We use a demographic approach to quantify fitness and test for selection on life history traits in local versus lower‐elevation populations and in normal versus drought years to test the potential for up‐slope migration and phenotypic selection to alter the distribution of key life history traits in montane environments. We find that lower‐elevation populations tend to outperform local populations, confirming the potential for up‐slope migration. Although selection generally favored some local montane traits, including larger flowers and larger stem size at flowering, drought conditions tended to select for earlier flowering typical of lower‐elevation genotypes. Taken together, this suggests that monkeyflower lineages moving upward in elevation could experience selection for novel trait combinations, particularly under warmer and drier conditions that are predicted to occur with continued climate change.     

Life‐history traits and physiological limits of the alpine fly Drosophila nigrosparsa (Diptera: Drosophilidae): A comparative study

Interspecific variation in life‐history traits and physiological limits can be linked to the environmental conditions species experience, including climatic conditions. As alpine environments are particularly vulnerable under climate change, we focus on the montane‐alpine fly Drosophila nigrosparsa. Here, we characterized some of its life‐history traits and physiological limits and compared these with those of other drosophilids, namely Drosophila hydei, Drosophila melanogaster, and Drosophila obscura. We assayed oviposition rate, longevity, productivity, development time, larval competitiveness, starvation resistance, and heat and cold tolerance. Compared with the other species assayed, D. nigrosparsa is less fecund, relatively long‐living, starvation susceptible, cold adapted, and surprisingly well heat adapted. These life‐history characteristics provide insights into invertebrate adaptations to alpine conditions which may evolve under ongoing climate change.     

Pace‐of‐life: Relationships among locomotor activity,life history,and circadian rhythm in the assassin bug,Amphibolus venator

The pace‐of‐life syndrome (POLS) hypothesis means that animal behavior is correlated with life history strategies. Studies have reported that the free‐running period of the circadian rhythm (length of the period) is correlated with life history strategies in some animals. Although the length of the circadian rhythm may be associated with the POLS hypothesis, few studies have investigated the relationships among animal behavior, life history traits, and circadian rhythm. We tested the POLS hypothesis in the assassin bug, Amphibolus venator, which shows individual variation in locomotor activity. We found higher repeatability of differences in locomotor activity between individuals. Moreover, we found a trade‐off between locomotor activity and developmental period such that active individuals developed faster. However, locomotor activity was not correlated with the length of the circadian rhythm in A. venator. Therefore, this study suggests that the length of the circadian rhythm in A. venator does not support the POLS hypothesis.     

Advances in finding Alba: the locus affecting life history and color polymorphism in a Colias butterfly

Although alternative life‐history strategies exist within many populations, very little is known about their genetic basis and mechanistic insight into these traits could greatly advance the understanding of eco‐evolutionary dynamics. Many species of butterfly within the genus Colias exhibit a sex‐limited wing colour polymorphism, called Alba, which is correlated with an alternative life‐history strategy. Here, we have taken the first steps in localizing the region carrying Alba in Colias croceus, a species with no genomic resources, by generating whole genome sequence of a single Alba mother and two sequencing pools, one for her Alba and another for her orange, offspring. These data were used in a bulk‐segregant analysis wherein SNPs fulfilling the Mendelian inheritance expectations of Alba were identified. Then, using the conserved synteny in Lepidoptera, the Alba locus was assigned to chromosome 15 in Bombyx mori. We then identified candidate regions within the chromosome by investigating the distribution of Alba SNPs along the chromosome and the difference in nucleotide diversity in exons between the two pools. A region spanning ~ 5.7 Mbp at the 5′ end of the chromosome was identified as likely to contain the Alba locus. These insights set the stage for more detailed genomic scans and mapping of the Alba phenotype, and demonstrate an efficient use of genomic resources in a novel species.     

Effects of variation in resource acquisition during different stages of the life cycle on life‐history traits and trade‐offs in a burying beetle

Individual variation in resource acquisition should have consequences for life‐history traits and trade‐offs between them because such variation determines how many resources can be allocated to different life‐history functions, such as growth, survival and reproduction. Since resource acquisition can vary across an individual's life cycle, the consequences for life‐history traits and trade‐offs may depend on when during the life cycle resources are limited. We tested for differential and/or interactive effects of variation in resource acquisition in the burying beetle Nicrophorus vespilloides. We designed an experiment in which individuals acquired high or low amounts of resources across three stages of the life cycle: larval development, prior to breeding and the onset of breeding in a fully crossed design. Resource acquisition during larval development and prior to breeding affected egg size and offspring survival, respectively. Meanwhile, resource acquisition at the onset of breeding affected size and number of both eggs and offspring. In addition, there were interactive effects between resource acquisition at different stages on egg size and offspring survival. However, only when females acquired few resources at the onset of breeding was there evidence for a trade‐off between offspring size and number. Our results demonstrate that individual variation in resource acquisition during different stages of the life cycle has important consequences for life‐history traits but limited effects on trade‐offs. This suggests that in species that acquire a fixed‐sized resource at the onset of breeding, the size of this resource has larger effects on life‐history trade‐offs than resources acquired at earlier stages.     

Colonisation of toxic environments drives predictable life‐history evolution in livebearing fishes (Poeciliidae)

New World livebearing fishes (family Poeciliidae) have repeatedly colonised toxic, hydrogen sulphide‐rich waters across their natural distribution. Physiological considerations and life‐history theory predict that these adverse conditions should favour the evolution of larger offspring. Here, we examined nine poeciliid species that independently colonised toxic environments, and show that these fishes have indeed repeatedly evolved much larger offspring size at birth in sulphidic waters, thus uncovering a widespread pattern of predictable evolution. However, a second pattern, only indirectly predicted by theory, proved additionally common: a reduction in the number of offspring carried per clutch (i.e. lower fecundity). Our analyses reveal that this secondary pattern represents a mere consequence of a classic life‐history trade‐off combined with strong selection on offspring size alone. With such strong natural selection in extreme environments, extremophile organisms may commonly exhibit multivariate phenotypic shifts even though not all diverging traits necessarily represent adaptations to the extreme conditions.     

Remarkable life history polymorphism may be evolving under divergent selection in the silverleaf sunflower

Substantial intraspecific variation in life history is rare and potentially a signal of incipient ecological speciation, if variation is driven by geographically heterogenous natural selection. We present the first report of extensive life history polymorphism in Helianthus argophyllus, the silverleaf sunflower, and examine evidence for its evolution by divergent selection. In 18 populations sampled from across the species range and grown in a common garden, most quantitative traits covaried such that individuals could be assigned to two distinct life history syndromes: tall and late flowering with small initial flowerheads, or short and early flowering with larger initial flowerheads. Helianthus argophyllus exhibits regional genetic structure, but this population structure does not closely correspond with patterns of phenotypic variation. The early‐flowering syndrome is primarily observed in populations from coastal barrier islands, while populations from the nearby mainland coast, although geographically and genetically close, are primarily late flowering. Additionally, several traits are more differentiated among regions than expected based on neutral genetic divergence (Q_ST > F_ST), including the first principal component score corresponding with life history syndrome. This discordance between patterns of phenotypic and genetic variation suggests that divergent selection is driving genetic differences in life history across the species range. If so, the silverleaf sunflower may be in early stages of ecological speciation.     

Gene expression under chronic heat stress in populations of the mustard hill coral (Porites astreoides) from different thermal environments

Recent evidence suggests that corals can acclimatize or adapt to local stress factors through differential regulation of their gene expression. Profiling gene expression in corals from diverse environments can elucidate the physiological processes that may be responsible for maximizing coral fitness in their natural habitat and lead to a better understanding of the coral's capacity to survive the effects of global climate change. In an accompanying paper, we show that Porites astreoides from thermally different reef habitats exhibit distinct physiological responses when exposed to 6 weeks of chronic temperature stress in a common garden experiment. Here, we describe expression profiles obtained from the same corals for a panel of 9 previously reported and 10 novel candidate stress response genes identified in a pilot RNA‐Seq experiment. The strongest expression change was observed in a novel candidate gene potentially involved in calcification, SLC26, a member of the solute carrier family 26 anion exchangers, which was down‐regulated by 92‐fold in bleached corals relative to controls. The most notable signature of divergence between coral populations was constitutive up‐regulation of metabolic genes in corals from the warmer inshore location, including the gluconeogenesis enzymes pyruvate carboxylase and phosphoenolpyruvate carboxykinase and the lipid beta‐oxidation enzyme acyl‐CoA dehydrogenase. Our observations highlight several molecular pathways that were not previously implicated in the coral stress response and suggest that host management of energy budgets might play an adaptive role in holobiont thermotolerance.     

An experimental heat wave changes immune defense and life history traits in a freshwater snail

The predicted increase in frequency and severity of heat waves due to climate change is expected to alter disease dynamics by reducing hosts' ability to resist infections. This could take place via two different mechanisms: (1) through general reduction in hosts' performance under harsh environmental conditions and/or (2) through altered resource allocation that reduces expression of defense traits in order to maintain other traits. We tested these alternative hypotheses by measuring the effect of an experimental heat wave (25 vs. 15°C) on the constitutive level of immune defense (hemocyte concentration, phenoloxidase [PO]‐like activity, antibacterial activity of hemolymph), and life history traits (growth and number of oviposited eggs) of the great pond snail Lymnaea stagnalis. We also manipulated the exposure time to high temperature (1, 3, 5, 7, 9, or 11 days). We found that if the exposure to high temperature lasted <1 week, immune function was not affected. However, when the exposure lasted longer than that, the level of snails' immune function (hemocyte concentration and PO‐like activity) was reduced. Snails' growth and reproduction increased within the first week of exposure to high temperature. However, longer exposures did not lead to a further increase in cumulative reproductive output. Our results show that short experimental heat waves do not alter immune function but lead to plastic responses that increase snails' growth and reproduction. Thus, although the relative expression of traits changes, short experimental heat waves do not impair snails' defenses. Negative effects on performance get pronounced when the heat waves are prolonged suggesting that high performance cannot be maintained over long time periods. This ultimately reduces the levels of defense traits.     

The molecular basis of invasiveness: differences in gene expression of native and introduced common ragweed (Ambrosia artemisiifolia) in stressful and benign environments

Although the evolutionary and ecological processes that contribute to plant invasion have been the focus of much research, investigation into the molecular basis of invasion is just beginning. Common ragweed (Ambrosia artemisiifolia) is an annual weed native to North America and has been introduced to Europe where it has become invasive. Using a custom‐designed NimbleGen oligoarray, we examined differences in gene expression between five native and six introduced populations of common ragweed in three different environments (control, light stress and nutrient stress), as well as two different time points. We identified candidate genes that may contribute to invasiveness in common ragweed based on differences in expression between native and introduced populations from Europe. Specifically, we found 180 genes where range explained a significant proportion of the variation in gene expression and a further 103 genes with a significant range by treatment interaction. Several of these genes are potentially involved in the metabolism of secondary compounds, stress response and the detoxification of xenobiotics. Previously, we found more rapid growth and greater reproductive success in introduced populations, particularly in benign and competitive (light stress) environments, and many of these candidate genes potentially underlie these growth differences. We also found expression differences among populations within each range, reflecting either local adaptation or neutral processes, although no associations with climate or latitude were identified. These data provide a first step in identifying genes that are involved with introduction success in an aggressive annual weed.     

Dissecting the role of a large chromosomal inversion in life history divergence throughout the Mimulus guttatus species complex

Chromosomal inversions can play an important role in adaptation, but the mechanism of their action in many natural populations remains unclear. An inversion could suppress recombination between locally beneficial alleles, thereby preventing maladaptive reshuffling with less‐fit, migrant alleles. The recombination suppression hypothesis has gained much theoretical support but empirical tests are lacking. Here, we evaluated the evolutionary history and phenotypic effects of a chromosomal inversion which differentiates annual and perennial forms of Mimulus guttatus. We found that perennials likely possess the derived orientation of the inversion. In addition, this perennial orientation occurs in a second perennial species, M. decorus, where it is strongly associated with life history differences between co‐occurring M. decorus and annual M. guttatus. One prediction of the recombination suppression hypothesis is that loci contributing to local adaptation will predate the inversion. To test whether the loci influencing perenniality pre‐date this inversion, we mapped QTLs for life history traits that differ between annual M. guttatus and a more distantly related, collinear perennial species, M. tilingii. Consistent with the recombination suppression hypothesis, we found that this region is associated with life history in the absence of the inversion, and this association can be broken into at least two QTLs. However, the absolute phenotypic effect of the LG8 inversion region on life history is weaker in M. tilingii than in perennials which possess the inversion. Thus, while we find support for the recombination suppression hypothesis, the contribution of this inversion to life history divergence in this group is likely complex.     

昆虫生活史的科学记述方法

文中介绍了昆虫学著述中常用的昆虫生活史表达方法 ,简单地讨论了有关方法的优缺点     

Misregulation of spermatogenesis genes in Drosophila hybrids is lineage‐specific and driven by the combined effects of sterility and fast male regulatory divergence

Hybrid male sterility is a common outcome of crosses between different species. Gene expression studies have found that a number of spermatogenesis genes are differentially expressed in sterile hybrid males, compared with parental species. Late‐stage sperm development genes are particularly likely to be misexpressed, with fewer early‐stage genes affected. Thus, a link has been posited between misexpression and sterility. A more recent alternative explanation for hybrid gene misexpression has been that it is independent of sterility and driven by divergent evolution of male‐specific regulatory elements between species (faster male hypothesis). The faster male hypothesis predicts that misregulation of spermatogenesis genes should be independent of sterility and approximately the same in both hybrids, whereas sterility should only affect gene expression in sterile hybrids. To test the faster male hypothesis vs. the effect of sterility on gene misexpression, we analyse spermatogenesis gene expression in different species pairs of the Drosophila phylogeny, where hybrid male sterility occurs in only one direction of the interspecies cross (i.e. unidirectional sterility). We find significant differences among genes in misexpression with effects that are lineage‐specific and caused by sterility or fast male regulatory divergence.