Genome-wide population genetic analysis identifies evolutionary forces establishing continuous population divergence

Elucidating the mechanism shaping the spatial variations of traits has long been a central concern of evolutionary biologists. Geographic clines of allele/morph frequencies along environmental gradients are suggested to be established and maintained by the balancing of two opposing evolutionary forces, namely selection that generates spatial differentiation in morph frequencies, and selection and/or stochastic factors that lead to the coexistence of multiple morphs within a population. Thus, testing for both selection and stochastic factors is necessary for a comprehensive understanding of the mechanism underlying clinal variation in morph/allele frequency in natural populations. Here, I identified the evolutionary forces responsible for clinal variation of color morph frequency in Ischnura senegalensis by comparing the population divergence of putatively neutral loci generated by high-throughput next-generation sequencing (F _STn) with that of the putative color locus (F _STc). No strong correlation was observed between F _STn and F _STc, suggesting that stochastic factors contribute less to color-locus population divergence. F _STc was less than F _STn between populations exposed to similar environmental conditions, but greater than F _STn between populations exposed to different environmental conditions, suggesting that both balancing selection and divergent selection act on the color locus. Therefore, two antagonistic selection factors rather than stochastic and historical factors contribute to establishing the clinal variation of morph frequency in I. senegalensis.     

Back to basics: using colour polymorphisms to study evolutionary processes

Here, I suggest that colour polymorphic study systems have been underutilized to answer general questions about evolutionary processes, such as morph frequency dynamics between generations and population divergence in morph frequencies. Colour polymorphisms can be used to study fundamental evolutionary processes like frequency‐dependent selection, gene flow, recombination and correlational selection for adaptive character combinations. However, many previous studies of colour polymorphism often suffer from weak connections to population genetic theory. I argue that too much focus has been directed towards noticeable visual traits (colour) at the expense of understanding the evolutionary processes shaping genetic variation and covariation associated with polymorphisms in general. There is thus no need for a specific evolutionary theory for colour polymorphisms beyond the general theory of the maintenance of polymorphisms in spatially or temporally variable environments or through positive or negative frequency‐dependent selection. I outline an integrative research programme incorporating these processes and suggest some fruitful avenues in future investigations of colour polymorphisms.     

Geographic variation in animal colour polymorphisms and its role in speciation

Polymorphic species, in which multiple variants coexist within a population, are often used as model systems in evolutionary biology. Recent research has been dominated by the hypothesis that polymorphism can be a precursor to speciation. To date, the majority of research regarding polymorphism and speciation has focused on whether polymorphism is maintained within a population or whether morphs within populations may diverge to form separate species (sympatric speciation); however, the geographical context of speciation in polymorphic systems is likely to be both diverse and complex. In this review, we draw attention to the geographic variation in morph composition and frequencies that characterises many, if not most polymorphic species. Recent theoretical and empirical developments suggest that such variation in the number, type and frequency of morphs present among populations can increase the probability of speciation. Thus, the geographical context of a polymorphism requires a greater research focus. Here, we review the prevalence, causes and evolutionary consequences of geographic variation in polymorphism in colour‐polymorphic animal species. The prevalence and nature of geographic variation in polymorphism suggests that polymorphism may be a precursor to and facilitate speciation more commonly than appreciated previously. We argue that a better understanding of the processes generating geographic variation in polymorphism is vital to understanding how polymorphism can promote speciation.     

Range limits,large‐scale biogeographic variation,and localized evolutionary dynamics in a polymorphic damselfly

Studies of heritable colour polymorphisms allow investigators to track the genetic dynamics of natural populations. By comparing polymorphic populations over large geographic areas and across generations, issues about both morph stability and evolutionary dynamics can be addressed, increasing our understanding of the potential mechanisms maintaining genetic polymorphisms. In the present study, we investigated population morph frequencies in a sex‐limited heritable colour polymorphic damselfly (Ischnura elegans, Vander Linden), with three discrete female morphs. We compared the frequencies of these three female morphs in 120 different populations from ten European countries at differing latitudes and longitudes. There were pronounced differences in morph frequencies both across the entire European biogeographic range, as well as at a smaller scale within regions. We also found considerable between‐population variation at the local scale within regions, particularly at the edges of the range of this species. We discuss these findings in the context of recent models of adaptive population divergence along the range of a species. This polymorphism is thus highly dynamic, with stable morph frequencies at the core of the species range but fluctuating morph dynamics at the range limits. We finish with a discussion of how local interactions and climatic factors can be expected to have a strong influence on the biogeographic patterns in this species and other sexually selected polymorphisms. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 775–785.     

The island rule and a research agenda for studying ecogeographical patterns

We are currently experiencing a resurgence of interest in ecogeographical rules, which describe general trends in morphology and related traits along geographical gradients. In order to develop a more comprehensive understanding of the generality and underlying causal mechanisms for these patterns, we recommend a new, more integrated research agenda. In particular, we recommend studies that simultaneously consider different clines in morphology, geographical ranges and diversity as intricately related phenomena; all being ecological, evolutionary and biogeographical responses of organisms to selection regimes that vary non-randomly over space and time, and among species with different ecological and evolutionary histories.     

Alternative reproductive strategies and the maintenance of female color polymorphism in damselflies

Genetic polymorphisms are powerful model systems to study the maintenance of diversity in nature. In some systems, polymorphisms are limited to female coloration; these are thought to have arisen as a consequence of reducing male mating harassment, commonly resulting in negative frequency‐dependent selection on female color morphs. One example is the damselfly Ischnura elegans, which shows three female color morphs and strong sexual conflict over mating rates. Here, we present research integrating male tactics, and female evolutionary strategies (female mating behavior and morph‐specific female fecundity) in populations with different morph‐specific mating frequencies, to obtain an understanding of mating rates in nature that goes beyond the mere measure of color frequencies. We found that female morph behavior differed significantly among but not within morphs (i.e., female morph behavior was fixed). In contrast, male tactics were strongly affected by the female morph frequency in the population. Laboratory work comparing morph‐specific female fecundity revealed that androchrome females have lower fecundity than both of the gynochrome female morphs in the short term (3‐days), but over a 10‐day period one of the gynochrome female morphs became more fecund than either of the other morphs. In summary, our study found sex‐specific dynamics in response to different morph frequencies and also highlights the importance of studying morph‐specific fecundities across different time frames to gain a better understanding of the role of alternative reproductive strategies in the maintenance of female‐limited color polymorphism.     

ECOLOGICAL CONDITIONS AFFECT EVOLUTIONARY TRAJECTORY IN A PREDATOR–PREY SYSTEM

The arms race of adaptation and counter adaptation in predator–prey interactions is a fascinating evolutionary dynamic with many consequences, including local adaptation and the promotion or maintenance of diversity. Although such antagonistic coevolution is suspected to be widespread in nature, experimental documentation of the process remains scant, and we have little understanding of the impact of ecological conditions. Here, we present evidence of predator–prey coevolution in a long-term experiment involving the predatory bacterium Bdellovibrio bacteriovorus and the prey Pseudomonas fluorescens , which has three morphs (SM, FS, and WS). Depending on experimentally applied disturbance regimes, the predator–prey system followed two distinct evolutionary trajectories, where the prey evolved to be either super-resistant to predation (SM morph) without counter-adaptation by the predator, or moderately resistant (FS morph), specialized to and coevolving with the predator. Although predation-resistant FS morphs suffer a cost of resistance, the evolution of extreme resistance to predation by the SM morph was apparently unconstrained by other traits (carrying capacity, growth rate). Thus we demonstrate empirically that ecological conditions can shape the evolutionary trajectory of a predator–prey system.     

Dispatches from the neighborhood watch: Using citizen science and field survey data to document color morph frequency in space and time

Heritable color polymorphisms have a long history of study in evolutionary biology, though they are less frequently examined today than in the past. These systems, where multiple discrete, visually identifiable color phenotypes co‐occur in the same population, are valuable for tracking evolutionary change and ascertaining the relative importance of different evolutionary mechanisms. Here, we use a combination of citizen science data and field surveys in the Great Lakes region of North America to identify patterns of color morph frequencies in the eastern gray squirrel (Sciurus carolinensis). Using over 68,000 individual squirrel records from both large and small spatial scales, we identify the following patterns: (a) the melanistic (black) phenotype is often localized but nonetheless widespread throughout the Great Lakes region, occurring in all states and provinces sampled. (b) In Ohio, where intensive surveys were performed, there is a weak but significantly positive association between color morph frequency and geographic proximity of populations. Nonetheless, even nearby populations often had radically different frequencies of the melanistic morph, which ranged from 0% to 96%. These patterns were mosaic rather than clinal. (c) In the Wooster, Ohio population, which had over eight years of continuous data on color morph frequency representing nearly 40,000 records, we found that the frequency of the melanistic morph increased gradually over time on some survey routes but decreased or did not change over time on others. These differences were statistically significant and occurred at very small spatial scales (on the order of hundreds of meters). Together, these patterns are suggestive of genetic drift as an important mechanism of evolutionary change in this system. We argue that studies of color polymorphism are still quite valuable in advancing our understanding of fundamental evolutionary processes, especially when coupled with the growing availability of data from citizen science efforts.     

Do group dynamics affect colour morph clines during a range shift?

Species exhibiting colour polymorphism are thought to have an ecological advantage at the landscape scale, because spatial segregation of alternatively adapted ecotypes into diverse habitats can increase the species' niche breadth and thus confer greater geographic range size. However, morph frequencies are also influenced by intrapopulational processes such as frequency‐ or density‐dependent social interactions. To identify how social feedback may affect clinal variation in morph frequencies, we investigated reciprocal interactions between morph‐specific thermal tolerance, local climatic conditions and social environments, in the context of a colour‐morph frequency cline associated with a recent range expansion in blue‐tailed damselflies (Ischnura elegans) in Sweden. Cold tolerances of gynochromes (female‐like female morph) were positively correlated with local gynochrome frequencies, suggesting a positive frequency‐dependent fitness benefit. In contrast, androchrome (male‐mimic female morph) cold tolerances were improved following recent exposure to cold weather, suggesting a beneficial environmental acclimation effect. Thus, according to an environment‐matching hypothesis for clinal variation, androchrome frequencies should therefore increase towards the (cooler) range limit. In contrast to this prediction, gynochrome frequencies increased at the expanding range limit, consistent with a positive frequency‐dependent social feedback that is beneficial when invading novel climates. Our results suggest that when phenotypes or fitnesses are affected by interactions with conspecifics, beneficial social effects on environmental tolerances may (i) facilitate range shifts, and (ii) reverse or counteract typical patterns of intraspecific interactions and environment‐matching clines observed in stable populations observed over broader geographic scales.     

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

Abstract. 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.     

How chromosomal rearrangements shape adaptation and speciation: Case studies in Drosophila pseudoobscura and its sibling species Drosophila persimilis

The gene arrangements of Drosophila have played a prominent role in the history of evolutionary biology from the original quantification of genetic diversity to current studies of the mechanisms for the origin and establishment of new inversion mutations within populations and their subsequent fixation between species supporting reproductive barriers. This review examines the genetic causes and consequences of inversions as recombination suppressors and the role that recombination suppression plays in establishing inversions in populations as they are involved in adaptation within heterogeneous environments. This often results in the formation of clines of gene arrangement frequencies among populations. Recombination suppression leads to the differentiation of the gene arrangements which may accelerate the accumulation of fixed genetic differences among populations. If these fixed mutations cause incompatibilities, then inversions pose important reproductive barriers between species. This review uses the evolution of inversions in Drosophila pseudoobscura and D. persimilis as a case study for how inversions originate, establish and contribute to the evolution of reproductive isolation.     

Biogeographical survey identifies consistent alternative physiological optima and a minor role for environmental drivers in maintaining a polymorphism

The contribution of adaptive mechanisms in maintaining genetic polymorphisms is still debated in many systems. To understand the contribution of selective factors in maintaining polymorphism, we investigated large-scale (>1000 km) geographic variation in morph frequencies and fitness-related physiological traits in the damselfly Nehalennia irene. As fitness-related physiological traits, we investigated investment in immune function (phenoloxidase activity), energy storage and fecundity (abdomen protein and lipid content), and flight muscles (thorax protein content). In the first part of the study, our aim was to identify selective agents maintaining the large-scale spatial variation in morph frequencies. Morph frequencies varied considerably among populations, but, in contrast to expectation, in a geographically unstructured way. Furthermore, frequencies co-varied only weakly with the numerous investigated ecological parameters. This suggests that spatial frequency patterns are driven by stochastic processes, or alternatively, are consequence of highly variable and currently unidentified ecological conditions. In line with this, the investigated ecological parameters did not affect the fitness-related physiological traits differently in both morphs. In the second part of the study, we aimed at identifying trade-offs between fitness-related physiological traits that may contribute to the local maintenance of both colour morphs by defining alternative phenotypic optima, and test the spatial consistency of such trade-off patterns. The female morph with higher levels of phenoloxidase activity had a lower thorax protein content, and vice versa, suggesting a trade-off between investments in immune function and in flight muscles. This physiological trade-off was consistent across the geographical scale studied and supports widespread correlational selection, possibly driven by male harassment, favouring alternative trait combinations in both female morphs.     

NEGATIVE FREQUENCY‐DEPENDENT SELECTION IN FEMALE COLOR POLYMORPHISM OF A DAMSELFLY

Negative frequency‐dependent selection (NFDS) is one of the most powerful selective forces maintaining genetic polymorphisms in nature. Recently many prospective cases of polymorphisms by NFDS have been reported. Some of them are very complicated, although strongly supportive of the NFDS. Here we investigate NFDS in wild populations of the dimorphic damselfly Ischnura senegalensis, in which females occur as andromorphs and gynomorphs. Specifically, we (1) test fitness responses to morph frequencies, (2) built a simple population genetic model, and (3) compare the observed and predicted morph‐frequency dynamics. Fitnesses of the two morphs are an inverse function of its own frequency in a population, and are about equal when their frequencies are similar. Thus the conditions necessary for NFDS are satisfied. The long‐term field surveys show that the morph frequencies oscillate with a period of two generations. Morph frequencies in a small population undergo large oscillations whereas those in a large population do small oscillations. The demographic properties of the observed dynamics agree well with those of our model. This example is one of the simplest confirmed cases of NFDS maintaining genetic polymorphisms in nature.     

Aphid wing dimorphisms: linking environmental and genetic control of trait variation

Both genetic and environmental factors underlie phenotypic variation. While research at the interface of evolutionary and developmental biology has made excellent advances in understanding the contribution of genes to morphology, less well understood is the manner in which environmental cues are incorporated during development to influence the phenotype. Also virtually unexplored is how evolutionary transitions between environmental and genetic control of trait variation are achieved. Here, I review investigations into molecular mechanisms underlying phenotypic plasticity in the aphid wing dimorphism system. Among aphids, some species alternate between environmentally sensitive (polyphenic) and genetic (polymorphic) control of wing morph determination in their life cycle. Therefore, a traditional molecular genetic approach into understanding the genetically controlled polymorphism may provide a unique avenue into not only understanding the molecular basis of polyphenic variation in this group, but also the opportunity to compare and contrast the mechanistic basis of environmental and genetic control of similar dimorphisms.     

Genetic drift within a protected polymorphism: enigmatic variation in color-morph frequencies in the candy-stripe spider, Enoplognatha ovata

The candy-stripe spider, Enoplognatha ovata, exhibits a striking color polymorphism comprising three morphs. A number of lines of evidence strongly suggest that this polymorphism is maintained by natural selection: its presence in a sister species, E. latimana; the physical nature of the variation; the virtual lack of monomorphic populations; the highly consistent rank-order of morphs within populations; and the presence of large-scale clines associated with climatic variables. However, the absence of selection is equally strongly suggested by very local surveys of morph frequencies over space and time, perturbation experiments, and a variance in morph frequency between populations that is virtually independent of spatial scale. In addition, local spatial patterns in one study site (Nidderdale, Yorkshire, England) have been explained in terms of intermittent drift over half a century ago, a hypothesis supported here by the distributions of four other genetic markers (two allozyme and two visible polymorphisms). A heuristic model is suggested that reconciles these apparently contradictory messages regarding the importance of drift and selection in this system. It is proposed that when allele frequencies of the color morph redimita lie between approximately 0.05 and 0.3, the deltaq on q plot is very shallow, so that within this region, where the majority of populations lie, selection is weak and drift is the major force determining local morph frequencies. However, outside this range of frequencies, powerful selection acts to protect the polymorphism. This model may apply to polymorphisms in other species and explain why evidence of selection in natural populations is often elusive.     

Hormones in the city: endocrine ecology of urban birds

Urbanization dramatically changes the landscape, presenting organisms with novel challenges and often leading to reduced species diversity. Urban ecologists have documented numerous biotic and abiotic consequences of urbanization, such as altered climate, species interactions, and community composition, but we lack an understanding of the mechanisms underlying organisms' responses to urbanization. Here, I review findings from the nascent field of study of the endocrine ecology of urban birds. Thus far, no clear or consistent patterns have been revealed, but we do have evidence that urban habitat can shape endocrine traits, and that those traits might contribute to adaptation to the urban environment. I suggest strong approaches for future work addressing exciting questions about the role of endocrine traits in mediating responses to urbanization within species across the globe.     

Fruit colour polymorphism in Acacia ligulata: seed and seedling performance, clinal patterns, and chemical variation

Fruit colour polymorphisms are widespread in nature, but their ecological and evolutionary dynamics remain poorly understood. Here we examine Acacia ligulata, a shrub of the Australian arid zone which exhibits a red/orange/yellow aril colour polymorphism. We asked whether the polymorphism had a genetic basis; whether selection acted differentially on morphs during the seed and seedling stages; whether geographic variation in morph frequencies was correlated with environmental factors; and whether morphs differed in physical or chemical characteristics that might influence selection on them. When grown to maturity in a common greenhouse environment, maternal families of seeds showed phenotypic patterns consistent with biparental genetic control of the polymorphism. In contrast to other fruit-colour polymorphic species, progeny of A. ligulata morphs did not vary in rates of seedling emergence or survival in a common garden. Sampling along a 580 km transect revealed clinal variation in morph frequencies. Frequencies of the yellow morph decreased, and frequencies of the red morph increased, across a gradient of decreasing temperature and increasing rainfall. Morphs did not differ in seed mass, aril mass, or in profiles of fatty acids and flavonoids in either arils or seeds. However, morphs showed consistent differences in carotenoid profiles' and elemental content of arils, suggesting that selection by avian and insect seed dispersers, seed predators and herbivores should be investigated. These patterns indicate that both abiotic and biotic factors may contribute to selection on the A. ligulata polymorphism. This revised version was published online in August 2006 with corrections to the Cover Date.     

动物个性研究进展

"个性"是指不同时空条件下动物种群个体间行为的稳定差异。大量的理论和实验性研究表明,个性差异在动物界普遍存在,其是种群多度和分布、物种共存及群落构建的重要驱动因子。介绍了动物个性的概念、分类及衡量指标,将前人测量个性类型的方法加以总结;随后介绍了动物个性的生态学意义,尤其是个性对动物生活史策略、种群分布与多度、群落结构和动态、生态系统功能和过程以及疾病与信息传播等的影响。在此基础上,进一步分析了在人类活动增加等全球变化背景下,动物个性如何调控动物个体行为、种群和群落动态对这些环境变化的响应。阐述了动物个性的形成与维持机制,并对未来的研究方向进行了展望。     

Viability,behavior, and color expression in the offspring of matings between common wall lizard Podarcis muralis color morphs

Color polymorphisms are widely studied to identify the mechanisms responsible for the origin and maintenance of phenotypic variability in nature. Two of the mechanisms of balancing selection currently thought to explain the long-term persistence of polymorphisms are the evolution of alternative phenotypic optima through correlational selection on suites of traits including color and heterosis. Both of these mechanisms can generate differences in offspring viability and fitness arising from different morph combinations. Here, we examined the effect of parental morph combination on fertilization success, embryonic viability, newborn quality, antipredator, and foraging behavior, as well as inter-annual survival by conducting controlled matings in a polymorphic lacertid Podarcis muralis, where color morphs are frequently assumed to reflect alternative phenotypic optima (e.g., alternative reproductive strategies). Juveniles were kept in outdoor tubs for a year in order to study inter-annual growth, survival, and morph inheritance. In agreement with a previous genome-wide association analysis, morph frequencies in the year-old juveniles matched the frequencies expected if orange and yellow expressions depended on recessive homozygosity at 2 separate loci. Our findings also agree with previous literature reporting higher reproductive output of heavy females and the higher overall viability of heavy newborn lizards, but we found no evidence for the existence of alternative breeding investment strategies in female morphs, or morph-combination effects on offspring viability and behavior. We conclude that inter-morph breeding remains entirely viable and genetic incompatibilities are of little significance for the maintenance of discrete color morphs in P. muralis from the Pyrenees.     

Molecular and quantitative genetic differentiation across Europe in yellow dung flies

Relating geographic variation in quantitative traits to underlying population structure is crucial for understanding processes driving population differentiation, isolation and ultimately speciation. Our study represents a comprehensive population genetic survey of the yellow dung fly Scathophaga stercoraria, an important model organism for evolutionary and ecological studies, over a broad geographic scale across Europe (10 populations from the Swiss Alps to Iceland). We simultaneously assessed differentiation in five quantitative traits (body size, development time, growth rate, proportion of diapausing individuals and duration of diapause), to compare differentiation in neutral marker loci (F(ST)) to that of quantitative traits (Q(ST)). Despite long distances and uninhabitable areas between sampled populations, population structuring was very low but significant (F(ST) = 0.007, 13 microsatellite markers; F(ST) = 0.012, three allozyme markers; F(ST) = 0.007, markers combined). However, only two populations (Iceland and Sweden) showed significant allelic differentiation to all other populations. We estimated high levels of gene flow [effective number of migrants (Nm) = 6.2], there was no isolation by distance, and no indication of past genetic bottlenecks (i.e. founder events) and associated loss of genetic diversity in any northern or island population. In contrast to the low population structure, quantitative traits were strongly genetically differentiated among populations, following latitudinal clines, suggesting that selection is responsible for life history differentiation in yellow dung flies across Europe.