Pattern and process: evidence for the evolution of photosynthetic traits in natural populations

The patterns of interspecific variation identified by comparative studies provide valuable hypotheses about the role of physiological traits in evolutionary adaptation. This review covers tests of these hypotheses for photosynthetic traits that have used a microevolutionary perspective to characterize physiological variation among and within populations. Studies of physiological differentiation among populations show that evolutionary divergence in photosynthetic traits is common within species, and has a pattern that supports many adaptive hypotheses. These among-population studies imply that selection has influenced photosynthetic traits in some way, but they are not designed to identify the traits targeted by selection or the environmental agents that cause selection. Analyses of genetic and phenotypic variation within populations address these questions. Studies that have quantified genetic variation within populations show that levels of heritable variation can be adequate for evolutionary change in photosynthetic traits. Other studies have measured phenotypic selection for these traits by analyzing how the variation within populations is correlated with fitness. This work has shown that selection for photosynthetic traits may often operate indirectly via correlations with other traits, and emphasizes the importance of viewing the phenotype as an integrated function of growth, morphology, life-history and physiology. We also outline some methodological problems that may be encountered for ecophysiological traits by these types of studies, provide some potential solutions, and discuss future directions for the field of plant evolutionary ecophysiology.     

Sexual Antagonism,Temporally Fluctuating Selection,and Variable Dominance Affect a Regulatory Polymorphism in Drosophila melanogaster

Understanding how genetic variation is maintained within species is a major goal of evolutionary genetics that can shed light on the preservation of biodiversity. Here, we examined the maintenance of a regulatory single-nucleotide polymorphism (SNP) of the X-linked Drosophila melanogaster gene fezzik. The derived variant at this site is at intermediate frequency in many worldwide populations but absent in populations from the ancestral species range in sub-Saharan Africa. We collected and genotyped wild-caught individuals from a single European population biannually over a period of 5 years, which revealed an overall difference in allele frequency between the sexes and a consistent change in allele frequency across seasons in females but not in males. Modeling based on the observed allele and genotype frequencies suggested that both sexually antagonistic and temporally fluctuating selection may help maintain variation at this site. The derived variant is predicted to be female-beneficial and mostly recessive; however, there was uncertainty surrounding our dominance estimates and long-term modeling projections suggest that it is more likely to be dominant. By examining gene expression phenotypes, we found that phenotypic dominance was variable and dependent upon developmental stage and genetic background, suggesting that dominance may be variable at this locus. We further determined that fezzik expression and genotype are associated with starvation resistance in a sex-dependent manner, suggesting a potential phenotypic target of selection. By characterizing the mechanisms of selection acting on this SNP, our results improve our understanding of how selection maintains genetic and phenotypic variation in natural populations.     

Does natural selection promote population divergence? A comparative analysis of population structure using amplified fragment length polymorphism markers and quantitative traits

Divergent natural selection is considered an important force in plant evolution leading to phenotypic differentiation between populations exploiting different environments. Extending an earlier greenhouse study of population differentiation in the selfing annual plant Senecio vulgaris, we estimated the degree of population divergence in several quantitative traits related to growth and life history and compared these estimates with those based on presumably neutral molecular markers (amplified fragment length polymorphisms; AFLPs). This approach allowed us to disentangle the effects of divergent selection from that of other evolutionary forces (e.g. genetic drift). Five populations were examined from each of two habitat types (ruderal and agricultural habitats). We found a high proportion of total genetic variance to be among populations, both for AFLP markers (phiST = 0.49) and for quantitative traits (range of QST: 0.26-0.77). There was a strong correlation between molecular and quantitative genetic differentiation between pairs of populations (Mantel's r = 0.59). However, estimates of population differentiation in several quantitative traits exceeded the neutral expectation (estimated from AFLP data), suggesting that divergent selection contributed to phenotypic differentiation, especially between populations from ruderal and agricultural habitats. Estimates of within-population variation in AFLP markers and quantitative genetic were poorly correlated, indicating that molecular marker data may be of limited value to predict the evolutionary potential of populations of S. vulgaris.     

Genetic variation in response to an indirect ecological effect

Indirect ecological effects (IEEs) are widespread and often as strong as the phenotypic effects arising from direct interactions in natural communities. Indirect effects can influence competitive interactions, and are thought to be important selective forces. However, the extent that selection arising from IEEs results in long-term evolutionary change depends on genetic variation underlying the phenotypic response-that is, a genotype-by-IEE interaction. We provide the first data on genetic variation in the response of traits to an IEE, and illustrate how such genetic variation might be detected and analysed. We used a model tri-trophic system to investigate the effect of host plants on two populations of predatory ladybirds through a clonal aphid herbivore. A split-family experimental design allowed us to estimate the effects of aphid host plant on ladybird traits (IEE) and the extent of genetic variation in ladybird predators for response to these effects (genotype-by-indirect environmental effect interaction). We found significant genetic variation in the response of ladybird phenotypes to the indirect effect of host plant of their aphid prey, demonstrating the potential for evolutionary responses to selection arising from the prey host.     

Which evolutionary processes influence natural genetic variation for phenotypic traits?

Although many studies provide examples of evolutionary processes such as adaptive evolution, balancing selection, deleterious variation and genetic drift, the relative importance of these selective and stochastic processes for phenotypic variation within and among populations is unclear. Theoretical and empirical studies from humans as well as natural animal and plant populations have made progress in examining the role of these evolutionary forces within species. Tentative generalizations about evolutionary processes across species are beginning to emerge, as well as contrasting patterns that characterize different groups of organisms. Furthermore, recent technical advances now allow the combination of ecological measurements of selection in natural environments with population genetic analysis of cloned QTLs, promising advances in identifying the evolutionary processes that influence natural genetic variation.     

High temperatures reveal cryptic genetic variation in a polymorphic female sperm storage organ

Variation in female reproductive morphology may play a decisive role in reproductive isolation by affecting the relative fertilization success of alternative male phenotypes. Yet, knowledge of how environmental variation may influence the development of the female reproductive tract and thus alter the arena of postcopulatory sexual selection is limited. Yellow dung fly females possess either three or four sperm storage compartments, a polymorphism with documented influence on sperm precedence. We performed a quantitative genetics study including 12 populations reared at three developmental temperatures complemented by extensive field data to show that warm developmental temperatures increase the frequency of females with four compartments, revealing striking hidden genetic variation for the polymorphism. Systematic genetic differentiation in growth rate and spermathecal number along latitude, and phenotypic covariance between the traits across temperature treatments suggest that the genetic architecture underlying the polymorphism is shaped by selection on metabolic rate. Our findings illustrate how temperature can modulate the preconditions for sexual selection by differentially exposing novel variation in reproductive morphology. This implies that environmental change may substantially alter the dynamics of sexual selection. We further discuss how temperature-dependent developmental plasticity may have contributed to observed rapid evolutionary transitions in spermathecal morphology.     

Compensatory Evolution and the Origins of Innovations

Cryptic genetic sequences have attenuated effects on phenotypes. In the classic view, relaxed selection allows cryptic genetic diversity to build up across individuals in a population, providing alleles that may later contribute to adaptation when co-opted—e.g., following a mutation increasing expression from a low, attenuated baseline. This view is described, for example, by the metaphor of the spread of a population across a neutral network in genotype space. As an alternative view, consider the fact that most phenotypic traits are affected by multiple sequences, including cryptic ones. Even in a strictly clonal population, the co-option of cryptic sequences at different loci may have different phenotypic effects and offer the population multiple adaptive possibilities. Here, we model the evolution of quantitative phenotypic characters encoded by cryptic sequences and compare the relative contributions of genetic diversity and of variation across sites to the phenotypic potential of a population. We show that most of the phenotypic variation accessible through co-option would exist even in populations with no polymorphism. This is made possible by a history of compensatory evolution, whereby the phenotypic effect of a cryptic mutation at one site was balanced by mutations elsewhere in the genome, leading to a diversity of cryptic effect sizes across sites rather than across individuals. Cryptic sequences might accelerate adaptation and facilitate large phenotypic changes even in the absence of genetic diversity, as traditionally defined in terms of alternative alleles.     

A test for the genetic basis of natural selection: an individual-based longitudinal study in a stream-dwelling fish

In addition to the well-studied evolutionary parameters of (1) phenotype-fitness covariance and (2) the genetic basis of phenotypic variation, adaptive evolution by natural selection requires that (3) fitness variation is effected by heritable genetic differences among individuals and (4) phenotype-fitness covariances must be, at least in part, underlain by genetic covariances. These latter two requirements for adaptive evolutionary change are relatively unstudied in natural populations. Absence of the latter requirements could explain stasis of apparently directionally selected heritable traits. We provide complementary analyses of selection and variation at phenotypic and genetic levels for juvenile growth rate in brook charr Salvelinus fontinalis in Freshwater River, Newfoundland, Canada. Contrary to the vast majority of reports in fish, we found very little viability selection of juvenile body size. Large body size appears nonetheless to be selectively advantageous via a relationship with early maturity. Genetic patterns in evolutionary parameters largely reflected phenotypic patterns. We have provided inference of selection based on longitudinal data, which are uncommon in high fecundity organisms. Furthermore we have provided a practicable framework for further studies of the genetic basis of natural selection.     

MAINTENANCE OF GENETIC VARIATION IN HUMAN PERSONALITY: TESTING EVOLUTIONARY MODELS BY ESTIMATING HERITABILITY DUE TO COMMON CAUSAL VARIANTS AND INVESTIGATING THE EFFECT OF DISTANT INBREEDING

Personality traits are basic dimensions of behavioral variation, and twin, family, and adoption studies show that around 30% of the between‐individual variation is due to genetic variation. There is rapidly growing interest in understanding the evolutionary basis of this genetic variation. Several evolutionary mechanisms could explain how genetic variation is maintained in traits, and each of these makes predictions in terms of the relative contribution of rare and common genetic variants to personality variation, the magnitude of nonadditive genetic influences, and whether personality is affected by inbreeding. Using genome‐wide single nucleotide polymorphism (SNP) data from > 8000 individuals, we estimated that little variation in the Cloninger personality dimensions (7.2% on average) is due to the combined effect of common, additive genetic variants across the genome, suggesting that most heritable variation in personality is due to rare variant effects and/or a combination of dominance and epistasis. Furthermore, higher levels of inbreeding were associated with less socially desirable personality trait levels in three of the four personality dimensions. These findings are consistent with genetic variation in personality traits having been maintained by mutation–selection balance.     

Molecular and quantitative trait variation within and among small fragmented populations of the endangered plant species Psilopeganum sinense

Background and Aims

Natural selection and genetic drift are important evolutionary forces in determining genetic and phenotypic differentiation in plant populations. The extent to which these two distinct evolutionary forces affect locally adaptive quantitative traits has been well studied in common plant and animal species. However, we know less about how quantitative traits respond to selection pressures and drift in endangered species that have small population sizes and fragmented distributions. To address this question, this study assessed the relative strengths of selection and genetic drift in shaping population differentiation of phenotypic traits in Psilopeganum sinense, a naturally rare and recently endangered plant species.

Methods

Population differentiation at five quantitative traits (Q_ST) obtained from a common garden experiment was compared with differentiation at putatively neutral microsatellite markers (F_ST) in seven populations of P. sinense. Q_ST estimates were derived using a Bayesian hierarchical variance component method.

Key Results

Trait-specific Q_ST values were equal to or lower than F_ST. Neutral genetic diversity was not correlated with quantitative genetic variation within the populations of P. sinense.

Conclusions

Despite the prevalent empirical evidence for Q_ST > F_ST, the results instead suggest a definitive role of stabilizing selection and drift leading to phenotypic differentiation among small populations. Three traits exhibited a significantly lower Q_ST relative to F_ST, suggesting that populations of P. sinense might have experienced stabilizing selection for the same optimal phenotypes despite large geographical distances between populations and habitat fragmentation. For the other two traits, Q_ST estimates were of the same magnitude as F_ST, indicating that divergence in these traits could have been achieved by genetic drift alone. The lack of correlation between molecular marker and quantitative genetic variation suggests that sophisticated considerations are required for the inference of conservation measures of P. sinense from neutral genetic markers.     

Phenotypic divergence among threespine stickleback that differ in nuptial coloration

By studying systems in their earliest stages of differentiation, we can learn about the evolutionary forces acting within and among populations and how those forces could contribute to reproductive isolation. Such an understanding would help us to better discern and predict how selection leads to the maintenance of multiple morphs within a species, rather than speciation. The postglacial adaptive radiation of the threespine stickleback (Gasterosteus aculeatus) is one of the best‐studied cases of evolutionary diversification and rapid, repeated speciation. Following deglaciation, marine stickleback have continually invaded freshwater habitats across the northern hemisphere and established resident populations that diverged innumerable times from their oceanic ancestors. Independent freshwater colonization events have yielded broadly parallel patterns of morphological differences in freshwater and marine stickleback. However, there is also much phenotypic diversity within and among freshwater populations. We studied a lesser‐known freshwater “species pair” found in southwest Washington, where male stickleback in numerous locations have lost the ancestral red sexual signal and instead develop black nuptial coloration. We measured phenotypic variation in a suite of traits across sites where red and black stickleback do not overlap in distribution and at one site where they historically co‐occurred. We found substantial phenotypic divergence between red and black morphs in noncolor traits including shape and lateral plating, and additionally find evidence that supports the hypothesis of sensory drive as the mechanism responsible for the evolutionary switch in color from red to black. A newly described third “mixed” morph in Connor Creek, Washington, differs in head shape and size from the red and black morphs, and we suggest that their characteristics are most consistent with hybridization between anadromous and freshwater stickleback. These results lay the foundation for future investigation of the underlying genetic basis of this phenotypic divergence as well as the evolutionary processes that may drive, maintain, or limit divergence among morphs.     

Neutral mutation as the source of genetic variation in life history traits

The mechanism underlying the maintenance of adaptive genetic variation is a long-standing question in evolutionary genetics. There are two concepts (mutation-selection balance and balancing selection) which are based on the phenotypic differences between alleles. Mutation - selection balance and balancing selection cannot properly explain the process of gene substitution, i.e. the molecular evolution of quantitative trait loci affecting fitness. I assume that such loci have non-essential functions (small effects on fitness), and that they have the potential to evolve into new functions and acquire new adaptations. Here I show that a high amount of neutral polymorphism at these loci can exist in real populations. Consistent with this, I propose a hypothesis for the maintenance of genetic variation in life history traits which can be efficient for the fixation of alleles with very small selective advantage. The hypothesis is based on neutral polymorphism at quantitative trait loci and both neutral and adaptive gene substitutions. The model of neutral - adaptive conversion (NAC) assumes that neutral alleles are not neutral indefinitely, and that in specific and very rare situations phenotypic (relative fitness) differences between them can appear. In this paper I focus on NAC due to phenotypic plasticity of neutral alleles. The important evolutionary consequence of NAC could be the increased adaptive potential of a population. Loci responsible for adaptation should be fast evolving genes with minimally discernible phenotypic effects, and the recent discovery of genes with such characteristics implicates them as suitable candidates for loci involved in adaptation.     

Morphometric differentiation across House Sparrow Passer domesticus populations in Finland in comparison with the neutral expectation for divergence

To understand the biology of organisms it is important to take into account the evolutionary forces that have acted on their constituent populations. Neutral genetic variation is often assumed to reflect variation in quantitative traits under selection, though with even low neutral divergence there can be substantial differentiation in quantitative genetic variation associated with locally adapted phenotypes. To study the relative roles of natural selection and genetic drift in shaping phenotypic variation, the levels of quantitative divergence based on phenotypes (P_ST) and neutral genetic divergence (F_ST) can be compared. Such a comparison was made between 10 populations of Finnish House Sparrows (n = 238 individuals) collected in 2009 across the whole country. Phenotypic variation in tarsus‐length, wing‐length, bill‐depth, bill‐length and body mass were considered and 13 polymorphic microsatellite loci were analysed to quantify neutral genetic variation. Calculations of P_ST were based on Markov‐Chain Monte Carlo Bayesian estimates of phenotypic variances across and within populations. The robustness of the conclusions of the P_ST–F_ST comparison was evaluated by varying the proportion of variation due to additive genetic effects within and across populations. Our results suggest that body mass is under directional selection, whereas the divergence in other traits does not differ from neutral expectations. These findings suggest candidate traits for considering gene‐based studies of local adaptation. The recognition of locally adapted populations may be of value in the conservation of this declining species.     

Strong artificial selection in the wild results in predicted small evolutionary change

Estimates of genetic variation and selection allow for quantitative predictions of evolutionary change, at least in controlled laboratory experiments. Natural populations are, however, different in many ways, and natural selection on heritable traits does not always result in phenotypic change. To test whether we were able to predict the evolutionary dynamics of a complex trait measured in a natural, heterogeneous environment, we performed, over an 8-year period, a two-way selection experiment on clutch size in a subdivided island population of great tits (Parus major). Despite strong artificial selection, there was no clear evidence for evolutionary change at the phenotypic level. Environmentally induced differences in clutch size among years are, however, large and can mask evolutionary changes. Indeed, genetic changes in clutch size, inferred from a statistical model, did not deviate systematically from those predicted. Although this shows that estimates of genetic variation and selection can indeed provide quantitative predictions of evolutionary change, also in the wild, it also emphasizes that demonstrating evolution in wild populations is difficult, and that the interpretation of phenotypic trends requires great care.     

Causes of male sexual trait divergence in introduced populations of guppies

Males from different populations of the same species often differ in their sexually selected traits. Variation in sexually selected traits can be attributed to sexual selection if phenotypic divergence matches the direction of sexual selection gradients among populations. However, phenotypic divergence of sexually selected traits may also be influenced by other factors, such as natural selection and genetic constraints. Here, we document differences in male sexual traits among six introduced Australian populations of guppies and untangle the forces driving divergence in these sexually selected traits. Using an experimental approach, we found that male size, area of orange coloration, number of sperm per ejaculate and linear sexual selection gradients for male traits differed among populations. Within populations, a large mismatch between the direction of selection and male traits suggests that constraints may be important in preventing male traits from evolving in the direction of selection. Among populations, however, variation in sexual selection explained more than half of the differences in trait variation, suggesting that, despite within‐population constraints, sexual selection has contributed to population divergence of male traits. Differences in sexual traits were also associated with predation risk and neutral genetic distance. Our study highlights the importance of sexual selection in trait divergence in introduced populations, despite the presence of constraining factors such as predation risk and evolutionary history.     

The molecular basis of an avian plumage polymorphism in the wild: a melanocortin-1-receptor point mutation is perfectly associated with the melanic plumage morph of the bananaquit, Coereba flaveola

BACKGROUND: Evolution depends on natural selection acting on phenotypic variation, but the genes responsible for phenotypic variation in natural populations of vertebrates are rarely known. The molecular genetic basis for plumage color variation has not been described in any wild bird. Bananaquits (Coereba flaveola) are small passerine birds that occur as two main plumage variants, a widespread yellow morph with dark back and yellow breast and a virtually all black melanic morph. A candidate gene for this color difference is the melanocortin-1 receptor (MC1R), a key regulator of melanin synthesis in feather melanocytes. RESULTS: We sequenced the MC1R gene from four Caribbean populations of the bananaquit; two populations of the yellow morph and two populations containing both the yellow morph and the melanic morph. A point mutation resulting in the replacement of glutamate with lysine was present in at least one allele of the MC1R gene in all melanic birds and was absent in all yellow morph birds. This substitution probably causes the color variation, as the same substitution is responsible for melanism in domestic chickens and mice. The evolutionary relationships among the MC1R haplotypes show that the melanic alleles on Grenada and St. Vincent had a single origin. The low prevalence of nonsynonymous substitutions among yellow haplotypes suggests that they have been under stabilizing selection, whereas strong selective constraint on melanic haplotypes is absent. CONCLUSIONS: We conclude that a mutation in the MC1R is responsible for the plumage polymorphism in a wild bird population and that the melanic MC1R alleles in Grenada and St. Vincent bananaquit populations have a single evolutionary origin from a yellow allele.     

Genotype by environment interactions in viability and developmental time in populations of cactophilic Drosophila

The genetic and ecological basis of viability and developmental time differences between Drosophila buzzatii and D. koepferae were analysed using the isofemale line technique. Several isofemale lines were sampled from pairs of allopatric/sympatric populations of each species. Flies were reared in media prepared with decaying tissues of two of the main natural cactus hosts of each species. This experimental design enabled us to evaluate the relative contribution of phenotypic plasticity, genetic variation and genotype by environment interaction (G x E) to total phenotypic variation for two fitness traits, viability and developmental time. Our results revealed significant G x E in both traits, suggesting that the maintenance of genetic variation can be explained, at least in part, by diversifying selection in different patches of a heterogeneous environment in both species. However, the relative importance of the factors involved in the G x E varied between traits and populations within species. For viability, the G x E can be mainly attributed to changes in the rank order of lines across cacti. However, the pattern was different for developmental time. In D. buzzatii the G x E can be mainly accounted for by changes in among line variance across cacti, whereas changes in the rank order of lines across cacti was the main component in D. koepferae. These dissimilar patterns of variation between traits and species suggest that the evolutionary forces shaping genetic variation for developmental time and viability vary between populations within species and between species.     

Genetic analysis of life-history constraint and evolution in a wild ungulate population

Trade-offs among life-history traits are central to evolutionary theory. In quantitative genetic terms, trade-offs may be manifested as negative genetic covariances relative to the direction of selection on phenotypic traits. Although the expression and selection of ecologically important phenotypic variation are fundamentally multivariate phenomena, the in situ quantification of genetic covariances is challenging. Even for life-history traits, where well-developed theory exists with which to relate phenotypic variation to fitness variation, little evidence exists from in situ studies that negative genetic covariances are an important aspect of the genetic architecture of life-history traits. In fact, the majority of reported estimates of genetic covariances among life-history traits are positive. Here we apply theory of the genetics and selection of life histories in organisms with complex life cycles to provide a framework for quantifying the contribution of multivariate genetically based relationships among traits to evolutionary constraint. We use a Bayesian framework to link pedigree-based inference of the genetic basis of variation in life-history traits to evolutionary demography theory regarding how life histories are selected. Our results suggest that genetic covariances may be acting to constrain the evolution of female life-history traits in a wild population of red deer Cervus elaphus: genetic covariances are estimated to reduce the rate of adaptation by about 40%, relative to predicted evolutionary change in the absence of genetic covariances. Furthermore, multivariate phenotypic (rather than genetic) relationships among female life-history traits do not reveal this constraint.     

Neutral markers, ecologically relevant traits, and the structure of genetic variation in Daphnia

Zooplankton, Daphnia in particular, are increasingly used as model organisms to investigate general evolutionary biological questions. I here discuss some recent insights into the patterns and processes determining genetic diversity within and genetic differentiation among natural populations of cyclically parthenogenetic Daphnia. I focus on three aspects: (1) the interplay of phenotypic plasticity and genetic polymorphism in explaining variability in ecologically relevant traits, (2) the patterns of genetic variation revealed by neutral markers and ecologically relevant traits, and (3) the evolutionary ecological importance of hybridization events in Daphnia. The need for studies on the evolutionary ecology of sexual reproduction and dispersal via ephippial eggs in Daphnia is stressed.     

Testing the molecular and evolutionary causes of a 'leapfrog' pattern of geographical variation in coloration

Understanding the mechanisms accounting for the evolution of phenotypic diversity is central to evolutionary biology. We use molecular and phenotypic data to test hypotheses for 'leapfrog' patterns of geographical variation, in which phenotypically similar, disjunct populations are separated by distinct populations of the same species. Phylogenetic reconstructions revealed independent evolution of melanic plumage characters in different populations in the Neotropical avian genus Arremon. Thus, phenotypic similarities between distant populations cannot be explained by close phylogenetic affinity. Nor can they be attributed to recurring mutations in the MC1R gene, a locus involved in melanic pigmentation. A coalescent analysis indicates that plumage traits have become fixed at a faster rate than expected under genetic drift, suggesting that selection underlies their repeated evolution. In contrast to views that genetic drift drives phenotypic differentiation in Neotropical montane birds, our results imply that geographical variation preceding speciation may reflect the action of deterministic selective processes.