Correlated evolution of life-history with size at maturity in Daphnia pulicaria: patterns within and between populations

Explaining the repeated evolution of similar sets of traits under similar environmental conditions is an important issue in evolutionary biology. The extreme alternative classes of explanations for correlated suites of traits are optimal adaptation and genetic constraint resulting from pleiotropy. Adaptive explanations presume that individual traits are free to evolve to their local optima and that convergent evolution represents particularly adaptive combinations of traits. Alternatively, if pleiotropy is strong and difficult to break, strong selection on one or a few particularly important characters would be expected to result in consistent correlated evolution of associated traits. If pleiotropy is common, we predict that the pattern of divergence among populations will consistently reflect the within-population genetic architecture. To test the idea that the multivariate life-history phenotype is largely a byproduct of strong selection on body size, we imposed divergent artificial selection on size at maturity upon two populations of the cladoceran Daphnia pulicaria, chosen on the basis of their extreme divergence in body size. Overall, the trajectory of divergence between the two natural populations did not differ from that predicted by the genetic architecture within each population. However, the pattern of correlated responses suggested the presence of strong pleiotropic constraints only for adult body size and not for other life-history traits. One trait, offspring size, appears to have evolved in a way different from that expected from the within-population genetic architecture and may be under stabilizing selection.     

Genetic variation in pleiotropy: differential epistasis as a source of variation in the allometric relationship between long bone lengths and body weight

Pleiotropy is an aspect of genetic architecture underlying the phenotypic covariance structure. The presence of genetic variation in pleiotropy is necessary for natural selection to shape patterns of covariation between traits. We examined the contribution of differential epistasis to variation in the intertrait relationship and the nature of this variation. Genetic variation in pleiotropy was revealed by mapping quantitative trait loci (QTLs) affecting the allometry of mouse limb and tail length relative to body weight in the mouse-inbred strain LG/J by SM/J intercross. These relationship QTLs (rQTLs) modify relationships between the traits affected by a common pleiotropic locus. We detected 11 rQTLs, mostly affecting allometry of multiple bones. We further identified epistatic interactions responsible for the observed allometric variation. Forty loci that interact epistatically with the detected rQTLs were identified. We demonstrate how these epistatic interactions differentially affect the body size variance and the covariance of traits with body size. We conclude that epistasis, by differentially affecting both the canalization and mean values of the traits of a pleiotropic domain, causes variation in the covariance structure. Variation in pleiotropy maintains evolvability of the genetic architecture, in particular the evolvability of its modular organization.     

Genetic architecture of traits associated with serpentine adaptation of Silene vulgaris

Serpentine soils provide a difficult substrate for plant colonization and growth and therefore represent an ideal system for studying the genetics of habitat adaptation and the evolution of plant-ecotypes. Using an F2 mapping population derived from an intraspecific cross between a serpentine and a nonserpentine ecotype of Silene vulgaris, the genetic architecture of seven morphological, physiological and life-history traits was explored. A quantitative trait locus (QTL) analysis identified 23 QTLs, 15 of which were classified as major QTLs. The observed genetic architecture suggests that traits potentially involved in habitat adaptation are controlled by few genes of major effect and have evolved under consistent directional selection. Several linkage groups harboured overlapping QTLs for different traits, which can be due to either pleiotropy or linkage. The potential roles of these factors and of the time available for habitat adaptation and ecological speciation on serpentine are discussed.     

Mapping phenotypic plasticity and genotype-environment interactions affecting life-history traits in Caenorhabditis elegans

Phenotypic plasticity and genotype-environment interactions (GEI) play an important role in the evolution of life histories. Knowledge of the molecular genetic basis of plasticity and GEI provides insight into the underlying mechanisms of life-history changes in different environments. We used a genomewide single-nucleotide polymorphism map in a recombinant N2 x CB4856 inbred panel of the nematode Caenorhabditis elegans to study the genetic control of phenotypic plasticity to temperature in four fitness-related traits, that is, age at maturity, fertility, egg size and growth rate. We mapped quantitative trait loci (QTL) for the respective traits at 12 and 24 degrees C, as well as their plasticities. We found genetic variation and GEI for age at maturity, fertility, egg size and growth rate. GEI in fertility and egg size was attributed to changes in rank order of reaction norms. In case of age at maturity and growth rate, GEI was caused mainly by differences in the among-line variance. In total, 11 QTLs were detected, five QTL at 12 degrees C and six QTL at 24 degrees C, which were associated with life-history traits. Five QTL associated with age at maturity, fertility and growth rate showed QTL x environment interaction. These colocalized with plasticity QTL for the respective traits suggesting allelic sensitivity to temperature. Further fine mapping, complementation analyses and gene silencing are planned to identify candidate genes underlying phenotypic plasticity for age at maturity, fertility and growth.     

Insular shifts and trade-offs in life-history traits in pond frogs in the Zhoushan Archipelago, China

Island and mainland populations of animal species often differ strikingly in life-history traits such as clutch size, egg size, total reproductive effort and body size. However, despite widespread recognition of insular shifts in these life-history traits in birds, mammals and reptiles, there have been no reports of such life-history shifts in amphibians. Furthermore, most studies have focused on one specific life-history trait without explicit consideration of coordinated evolution among these intimately linked life-history traits, and thus the relationships among these traits are poorly studied. Here we provide the first evidence of insular shifts and trade-offs in a coordinated suite of life-history traits for an amphibian species, the pond frog Rana nigromaculata . Life-history data were collected from eight islands in the Zhoushan Archipelago and neighboring mainland China. We found consistent, significant shifts in all life-history traits between mainland and island populations. Island populations had smaller clutch sizes, larger egg sizes, larger female body size and invested less in total reproductive effort than mainland populations. Significant negative relationships were found between egg size and clutch size and between egg size and total reproductive effort among frog populations after controlling for the effects of body size. Therefore, decreased reproductive effort and clutch size, larger egg size and body size in pond frogs on islands were selected through trade-offs as an overall life-history strategy. Our findings contribute to the formation of a broad, repeatable ecological generality for insular shifts in life-history traits across a range of terrestrial vertebrate taxa.     

Evolution of pleiotropic alleles for maturation and size as a consequence of predation

Understanding life-history evolution requires knowledge about genetic interactions, physiological mechanisms and the nature of selection. For platyfish, Xiphophorus maculatus, extensive information is available about genetic and physiological mechanisms influencing life-history traits. In particular, alleles at the pituitary locus have large and antagonistic effects on age and size at sexual maturation. To examine how predation affects the evolution of these antagonistic traits, I examined pituitary allele evolution in experimental populations differing in predation risk. A smaller size, earlier maturation allele increased in frequency when predators were absent, while a larger size, later maturation allele increased in frequency when predators were present. Thus, predation favours alleles for larger size, at the cost of later maturation and reproduction. These findings are interesting for several reasons. First, predation is often predicted to favour early reproduction at smaller sizes. Second, few studies have shown how selection acts on alleles that affect age and size at sexual maturation. Finally, many studies assume that trade-offs between these life-history traits result from antagonistic pleiotropy, with alleles that positively affect one trait negatively affecting another, yet this is rarely known. This study unequivocally demonstrates that genetically based trade-offs affect life-history evolution in platyfish.     

QUANTITATIVE GENETICS OF SURVIVAL AND GROWTH IN IMPATIENS CAPENSIS

When variation in life-history characters is caused by many genes of small effect, then quantitative-genetic parameters may quantify constraints on rate and direction of microevolutionary change. I estimated heritabilities and genetic correlations for 16 life-history and morphological characters in two populations of Impatiens capensis, a partially self-pollinating herbaceous annual. The Madison population had little or no additive genetic variance for any of these characters, while the Milwaukee population had significant narrowsense heritabilities and genetic correlations for several traits, including adult size, which is highly correlated with fitness. All genetic correlations among fitness components were positive, hence there is no evidence for antagonistic pleiotropy among these traits. Dissimilarity of heritabilities in the two populations supports theoretical predictions that long-term changes in genetic variance-covariance patterns may occur when population sizes are small and selection is strong, as may occur in many plant species.     

Pleiotropic quantitative trait loci contribute to population divergence in traits associated with life-history variation in Mimulus guttatus

Evolutionary biologists seek to understand the genetic basis for multivariate phenotypic divergence. We constructed an F2 mapping population (N = 539) between two distinct populations of Mimulus guttatus. We measured 20 floral, vegetative, and life-history characters on parents and F1 and F2 hybrids in a common garden experiment. We employed multitrait composite interval mapping to determine the number, effect, and degree of pleiotropy in quantitative trait loci (QTL) affecting divergence in floral, vegetative, and life-history characters. We detected 16 QTL affecting floral traits; 7 affecting vegetative traits; and 5 affecting selected floral, vegetative, and life-history traits. Floral and vegetative traits are clearly polygenic. We detected a few major QTL, with all remaining QTL of small effect. Most detected QTL are pleiotropic, implying that the evolutionary shift between these annual and perennial populations is constrained. We also compared the genetic architecture controlling floral trait divergence both within (our intraspecific study) and between species, on the basis of a previously published analysis of M. guttatus and M. nasutus. Eleven of our 16 floral QTL map to approximately the same location in the interspecific map based on shared, collinear markers, implying that there may be a shared genetic basis for floral divergence within and among species of Mimulus.     

Analysis of two components of flight using recombinant inbred lines of Drosophila melanogaster

Complex activities require precise coordination of their components for successful action. The genetic basis underlying coordination of traits may range from relatively static pleiotropic associations to more flexible genetic associations that recombine in phenotypes under continuous selective modification by the environment. Successful flight in insects depends on the precise integration of numerous component physiological processes. Here we examine the genetic basis of two of its components, flight duration and rate. To study flight we created recombinant inbred populations from stocks of this laboratory known for their significantly longer duration flights. A heritable basis for these traits was found and determined to be positively correlated between sexes. Correlations of flight length with rate were negative within sexes, suggesting a trade-off, but were significant in males only. Composite interval mapping using the recombinant inbred (RI2) design was used to locate the QTLs for these traits and test for pleiotropy. Four QTLs affecting duration or wing beat rate were found on chromosomes II and III. Tests for pleiotropy showed some effects on traits of QTLs were common to both sexes while others were sex-specific. No QTL was pleiotropic for both traits, suggesting that correlations between flight duration and rate of wing beat are determined by a combination of linkage and environmental factors.     

Identification of QTLs for eight agronomically important traits using an ultra-high-density map based on SNPs generated from high-throughput sequencing in sorghum under contrasting photoperiods

The productivity of sorghum is mainly determined by agronomically important traits. The genetic bases of these traits have historically been dissected and analysed through quantitative trait locus (QTL) mapping based on linkage maps with low-throughput molecular markers, which is one of the factors that hinder precise and complete information about the numbers and locations of the genes or QTLs controlling the traits. In this study, an ultra-high-density linkage map based on high-quality single nucleotide polymorphisms (SNPs) generated from low-coverage sequences (~0.07 genome sequence) in a sorghum recombinant inbred line (RIL) population was constructed through new sequencing technology. This map consisted of 3418 bin markers and spanned 1591.4 cM of genome size with an average distance of 0.5 cM between adjacent bins. QTL analysis was performed and a total of 57 major QTLs were detected for eight agronomically important traits under two contrasting photoperiods. The phenotypic variation explained by individual QTLs varied from 3.40% to 33.82%. The high accuracy and quality of this map was evidenced by the finding that genes underlying two cloned QTLs, Dw3 for plant height (chromosome 7) and Ma1 for flowering time (chromosome 6), were localized to the correct genomic regions. The close associations between two genomic regions on chromosomes 6 and 7 with multiple traits suggested the existence of pleiotropy or tight linkage. Several major QTLs for heading date, plant height, numbers of nodes, stem diameter, panicle neck length, and flag leaf width were detected consistently under both photoperiods, providing useful information for understanding the genetic mechanisms of the agronomically important traits responsible for the change of photoperiod.     

Circadian rhythm and time of mating in Bactrocera cucurbitae (Diptera: Tephritidae) selected for age at reproduction

Chrono-biological traits were changed by selecting for life-history traits via a genetic linkage controlling both time-related behavioural and life-history traits. Behavioural traits were compared between lines selected for young (Y-lines) and old (O-lines) age at reproduction in the melon fly, Bactrocera cucurbitae (Coquillett). Adults from O-lines, which survive longer than flies from Y-lines, mated later in the day and had a longer period of circadian rhythm in the locomotor activity than those from Y-lines. Flies from F(1) reciprocal crosses had an intermediate time of mating and periods of circadian rhythm between that of the parents, indicating a genetic basis to these traits. The presence of these behavioural differences across the selection lines indicates that chrono-biological traits exhibit correlated responses to selection on age at reproduction. The correlated responses in the behavioural traits to selection for life-history traits are discussed from two points of view: pleiotropy and inadvertent selection.     

Covariation in Insular Life-history Traits of the Rice Frog(Fejervarya limnocharis)in Eastern China

Although shifts in life-history traits of insular vertebrates, as compared with mainland populations, have been observed in many taxa, few studies have examined the relationships among individual life-history traits on islands. Lifehistory theory also predicts that there is a trade-off between body size and reproductive effort, and between egg size and clutch size. We surveyed the rice frog, Fejervarya limnocharis, on 20 islands within the Zhoushan Archipelago and two nearby sites on the mainland of China to compare differences in life-history traits and to explore relationships among those traits. Rice frog females reached a greater body size on half of the smaller islands among the total 20 surveyed islands, and larger egg size, decreased clutch size and reduced reproductive effort on most of the islands when compared to the two mainland sites. Insular body size was negatively correlated with reproductive effort. There was a negative correlation between egg size and clutch size. Results suggest that life-history theory provides a good explanation for co-variation between body size and reproductive effort, and between egg size and clutch size in rice frogs on the islands.     

Sociality as a life-history tactic of ground squirrels

Summary Multi-variate analysis of life-history traits of 18 species of burrowing sciurids indicates that reproductive effort is determined by body-size energetics. Other traits, such as age adult weight reached, age of dispersal, length of time of gestation, were significantly correlated with body size. A principal component analysis suggested that the complex of life-history traits could be reduced to four components: body size (=weight), seasonality, specific reproductive effort, and maturity. The variation in the sociality index was best explained by age of first reproduction and age adult weight reached. Generally, species are more social when large body size combined with a relatively short growing season is associated with delayed dispersal and occurs in those species typically breeding for the first time at age two or older. Sociality in these species may have evolved through retention of daughters within the maternal home range as a means of continuing reproductive investment beyond weaning.     

Bayesian mapping of quantitative trait loci for multiple complex traits with the use of variance components

Complex traits important for humans are often correlated phenotypically and genetically. Joint mapping of quantitative-trait loci (QTLs) for multiple correlated traits plays an important role in unraveling the genetic architecture of complex traits. Compared with single-trait analysis, joint mapping addresses more questions and has advantages for power of QTL detection and precision of parameter estimation. Some statistical methods have been developed to map QTLs underlying multiple traits, most of which are based on maximum-likelihood methods. We develop here a multivariate version of the Bayes methodology for joint mapping of QTLs, using the Markov chain-Monte Carlo (MCMC) algorithm. We adopt a variance-components method to model complex traits in outbred populations (e.g., humans). The method is robust, can deal with an arbitrary number of alleles with arbitrary patterns of gene actions (such as additive and dominant), and allows for multiple phenotype data of various types in the joint analysis (e.g., multiple continuous traits and mixtures of continuous traits and discrete traits). Under a Bayesian framework, parameters--including the number of QTLs--are estimated on the basis of their marginal posterior samples, which are generated through two samplers, the Gibbs sampler and the reversible-jump MCMC. In addition, we calculate the Bayes factor related to each identified QTL, to test coincident linkage versus pleiotropy. The performance of our method is evaluated in simulations with full-sib families. The results show that our proposed Bayesian joint-mapping method performs well for mapping multiple QTLs in situations of either bivariate continuous traits or mixed data types. Compared with the analysis for each trait separately, Bayesian joint mapping improves statistical power, provides stronger evidence of QTL detection, and increases precision in estimation of parameter and QTL position. We also applied the proposed method to a set of real data and detected a coincident linkage responsible for determining bone mineral density and areal bone size of wrist in humans.     

The genetic architecture of domestication in the chicken: effects of pleiotropy and linkage

The extent of pleiotropy and epistasis in quantitative traits remains equivocal. In the case of pleiotropy, multiple quantitative trait loci are often taken to be pleiotropic if their confidence intervals overlap, without formal statistical tests being used to ascertain if these overlapping loci are statistically significantly pleiotropic. Additionally, the degree to which the genetic correlations between phenotypic traits are reflected in these pleiotropic quantitative trait loci is often variable, especially in the case of antagonistic pleiotropy. Similarly, the extent of epistasis in various morphological, behavioural and life-history traits is also debated, with a general problem being the sample sizes required to detect such effects. Domestication involves a large number of trade-offs, which are reflected in numerous behavioural, morphological and life-history traits which have evolved as a consequence of adaptation to selective pressures exerted by humans and captivity. The comparison between wild and domestic animals allows the genetic analysis of the traits that differ between these population types, as well as being a general model of evolution. Using a large F(2) intercross between wild and domesticated chickens, in combination with a dense SNP and microsatellite marker map, both pleiotropy and epistasis were analysed. The majority of traits were found to segregate in 11 tight 'blocks' and reflected the trade-offs associated with domestication. These blocks were shown to have a pleiotropic 'core' surrounded by more loosely linked loci. In contrast, epistatic interactions were almost entirely absent, with only six pairs identified over all traits analysed. These results give insights both into the extent of such blocks in evolution and the development of domestication itself.     

Fine mapping dissects pleiotropic growth quantitative trait locus into linked loci

A recurring issue in studies of quantitative trait loci (QTLs) is whether QTLs that appear to have pleiotropic effects are indeed caused by pleiotropy at single loci or by linked QTLs. Previous work identified a QTL that affected tail length in mice and the lengths of various bones, including the humerus, ulna, femur, tibia, and mandible. The effect of this QTL on tail length has since been found to be due to multiple linked QTLs and so its apparently pleiotropic effects may have been due to linked QTLs with distinct effects. In the present study we examined a line of mice segregating only for a 0.94-Mb chromosomal region known to contain a subset of the QTLs influencing tail length. We measured a number of skeletal dimensions, including the lengths of the skull, mandible, humerus, ulna, femur, tibia, calcaneus, metatarsus, and a tail bone. The QTL region was found to have effects on the size of the mandible and length of the tail bone, with little or no effect on the other traits. Using a randomization approach, we rejected the null hypothesis that the QTL affected all traits equally, thereby demonstrating that the pleiotropic effects reported earlier were due to linked loci with distinct effects. This result underlines the possibility that seemingly pleiotropic effects of QTLs may frequently be due to linked loci and that high-resolution mapping will often be required to distinguish between pleiotropy and linkage.     

Spontaneous mutational correlations for life-history, morphological and behavioral characters in Caenorhabditis elegans

The pattern of mutational covariance among traits plays a central, but largely untested, role in many theories in evolutionary genetics. Here we estimate the pattern of phenotypic, environmental, and mutational correlations for a set of life-history, behavioral, and morphological traits using 67 self-fertilizing lines of Caenorhabditis elegans, each having independently experienced an average of 370 generations of spontaneous mutation accumulation. Bivariate relationships of mutational effects indicate the existence of extensive pleiotropy. We find that mutations may tend to produce manifold effects on suites of functionally related traits; however, our data do not support the idea of completely parcelated pleiotropy, in which functional units are separately affected by mutations. Positive net phenotypic and mutational correlations are common for life-history traits, with environmental correlations being comparatively smaller and of the same sign for most pairs of traits. Observed mutational correlations are shown to be higher than those produced by the chance accumulation of nonpleiotropic mutations in the same lines.     

The extent and genetic basis of phenotypic divergence in life history traits in Mimulus guttatus

Differential natural selection acting on populations in contrasting environments often results in adaptive divergence in multivariate phenotypes. Multivariate trait divergence across populations could be caused by selection on pleiotropic alleles or through many independent loci with trait‐specific effects. Here, we assess patterns of association between a suite of traits contributing to life history divergence in the common monkey flower, Mimulus guttatus, and examine the genetic architecture underlying these correlations. A common garden survey of 74 populations representing annual and perennial strategies from across the native range revealed strong correlations between vegetative and reproductive traits. To determine whether these multitrait patterns arise from pleiotropic or independent loci, we mapped QTLs using an approach combining high‐throughput sequencing with bulk segregant analysis on a cross between populations with divergent life histories. We find extensive pleiotropy for QTLs related to flowering time and stolon production, a key feature of the perennial strategy. Candidate genes related to axillary meristem development colocalize with the QTLs in a manner consistent with either pleiotropic or independent QTL effects. Further, these results are analogous to previous work showing pleiotropy‐mediated genetic correlations within a single population of M. guttatus experiencing heterogeneous selection. Our findings of strong multivariate trait associations and pleiotropic QTLs suggest that patterns of genetic variation may determine the trajectory of adaptive divergence.     

The fast-slow continuum in mammalian life history: an empirical reevaluation

Many life-history traits co-vary across species, even when body size differences are controlled for. This phenomenon has led to the concept of a "fast-slow continuum," which has been influential in both empirical and theoretical studies of life-history evolution. We present a comparative analysis of mammalian life histories showing that, for mammals at least, there is not a single fast-slow continuum. Rather, both across and within mammalian clades, the speed of life varies along at least two largely independent axes when body size effects are removed. One axis reflects how species balance offspring size against offspring number, while the other describes the timing of reproductive bouts.     

A nonparametric bootstrap method for testing close linkage vs. pleiotropy of coincident quantitative trait loci.

A novel method using the nonparametric bootstrap is proposed for testing whether a quantitative trait locus (QTL) at one chromosomal position could explain effects on two separate traits. If the single-QTL hypothesis is accepted, pleiotropy could explain the effect on two traits. If it is rejected, then the effects on two traits are due to linked QTLs. The method can be used in conjunction with several QTL mapping methods as long as they provide a straightforward estimate of the number of QTLs detectable from the data set. A selection step was introduced in the bootstrap procedure to reduce the conservativeness of the test of close linkage vs. pleiotropy, so that the erroneous rejection of the null hypothesis of pleiotropy only happens at a frequency equal to the nominal type I error risk specified by the user. The approach was assessed using computer simulations and proved to be relatively unbiased and robust over the range of genetic situations tested. An example of its application on a real data set from a saline stress experiment performed on a recombinant population of wheat (Triticum aestivum L. ) doubled haploid lines is also provided.