RESPONSES OF FLORAL TRAITS TO SELECTION ON PRIMARY SEXUAL INVESTMENT IN SPERGULARIA MARINA: THE BATTLE BETWEEN THE SEXES

Two widespread assumptions underlie theoretical models of the evolution of sex allocation in hermaphroditic species: (1) resource allocations to male and female function are heritable; and (2) there is an intrinsic, genetically based negative correlation between male and female reproductive function. These assumptions have not been adequately tested in wild species, although a few studies have detected either genetic variation in pollen and ovule production per flower or evidence of trade-offs between male and female investment at the whole plant level. It may also be argued, however, that in highly autogamous, perfect-flowered plant taxa that exhibit genetic variation in gamete production, strong stabilizing selection for an efficient pollen:ovule ratio should result in a positive correlation among genotypes with respect to mean ovule and mean pollen production per flower. Here we report the results of a three-generation artificial selection experiment conducted on a greenhouse population of the autogamous annual plant Spergularia marina. Starting with a base population of 1200 individuals, we conducted intense mass selection for two generations, creating four selected lines (high and low ovule production per flower; high and low anther production per flower) and a control line. By examining the direct and correlated responses of several floral traits to selection on gamete production per flower, we evaluated the expectations that primary sexual investment would exhibit heritable variation and that resource-sharing, variation in resource-garnering ability, or developmental constraints mold the genetic correlations expressed among floral organs. The observed direct and correlated responses to selection on male and female gamete production revealed significant heritabilities of both ovule and anther production per flower and a significant negative genetic correlation between them. When plants were selected for increased ovules per flower over two generations, ovule production increased and anther production declined relative to the control line. Among plants selected for decreased anthers per flower, we observed a decline in anther production and an increase in ovule production relative to the control line. In contrast, the lines selected for low ovules per flower and for high anthers per flower exhibited no evidence for significant genetic correlations between male and female primary investment. Correlated responses to selection also indicate a genetically based negative correlation between the production of normal versus developmentally abnormal anthers (staminoid organs); a positive correlation between the production of ovules versus staminoid organs; and a positive correlation between the production of anthers and petals. The negative relationship between male versus female primary investment supports classical sex allocation theory, although the asymmetrical correlated responses to selection indicate that this relationship is not always expressed.     

Genetics of sex allocation in Mimulus (Scrophulariaceae)

Theoretical models of the evolution of resource allocation patterns to male and female function make the assumption that there are inherent trade-offs between the two. Here we use a quantitative genetic approach to quantify trade-offs between male and female function and to determine whether plant populations could readily respond to natural selection by quantifying the amount of genetic variation for pollen and ovule production. Both intra- and interspecific crossing designs were applied to two populations of the predominantly outcrossing Mimulus guttatus and two populations of the highly selfing congener, M. micranthus. The only significant correlations observed among pollen number, pollen size and ovule number were positive. Positive genetic correlations among the traits were sometimes reduced after removing the effect of flower size but still no significant negative correlations were detected. These results suggest that positive correlations between pollen and ovule production may be due to the joint positive correlation of these characters with the resource pool available for pollen and ovule production, as reflected by flower size. Heritabilities were moderate to high for ovule production but low for pollen number and pollen size and suggest that responses to selection would differ between the two traits. Crosses between the species revealed that there are additional genetic factors contributing to differences between the two species for corolla width, vs. pollen:ovule ratio. This is consistent with the hypothesis that genetic variation for resource acquisition may in part be responsible for the overall lack of a negative correlation between pollen and ovule production and provides a genetic explanation for little evidence of trade-offs between sexual functions in Mimulus.     

Sexual dimorphism and the genetic potential for evolution of sex allocation in the gynodioecious plant, Schiedea salicaria

Sex allocation theory addresses how separate sexes can evolve from hermaphroditism but little is known about the genetic potential for shifts in sex allocation in flowering plants. We tested assumptions of this theory using the common currency of biomass and measurements of narrow-sense heritabilities and genetic correlations in Schiedea salicaria, a gynodioecious species under selection for greater differentiation of the sexes. Female (carpel) biomass showed heritable variation in both sexes. Male (stamen) biomass in hermaphrodites also had significant heritability, suggesting the potential for further evolution of dioecy. Significant positive genetic correlations between females and hermaphrodites in carpel mass may slow differentiation between the sexes. Within hermaphrodites, there were no negative genetic correlations between male and female biomass as assumed by models for the evolution of dioecy, suggesting that S. salicaria is capable of further changes in biomass allocation to male and female functions and evolution toward dioecy.     

SEX ALLOCATION IN THE MONOECIOUS HERB BEGONIA SEMIOVATA

Sex-allocation models predict that the evolution of self-fertilization should result in a reduced allocation to male function and pollinator attraction in plants. The evolution of sex allocation may be constrained by both functional and genetic factors, however. We studied sex allocation and genetic variation for floral sex ratio and other reproductive traits in a Costa Rica population of the monoecious, highly selfing annual Begonia semiovata. Data on biomass of floral structures, flower sex ratios, and fruit set in the source population were used to calculate the average proportion of reproductive allocation invested in male function. Genetic variation and genetic correlations for floral sex ratio and for floral traits related to male and female function were estimated from the greenhouse-grown progeny of field-collected maternal families. The proportion of reproductive biomass invested in male function was low (0.34 at flowering, and 0.07 for total reproductive allocation). Significant among-family variation was detected in the size (mass) of individual male and female flowers, in the proportion of male flowers produced, and in the proportion of total flower mass invested in male flowers. Significant among-family variation was also found in flower number per inflorescence, petal length of male and female flowers, and petal number of female flowers. Except for female petal length, we found no difference in the mean value of these characters between selfed and outcrossed progeny, indicating that, with the possible exception of female petal length, the among-family variation detected was not the result of variation among families in the level of inbreeding. Significant positive phenotypic and broad-sense genetic correlations were detected between the mass of individual male and female flowers, between male and female petal length, and between number of male and number of female flowers per inflorescence. The ratio of stamen-to-pistil mass (0.33) was low compared to published data for autogamous species with hermaphroditic flowers, suggesting that highly efficient selfing mechanisms may evolve in monoecious species. Our results indicate that the study population harbors substantial genetic variation for reproductive characters. The positive genetic correlation between investment in male and female flowers may reflect selection for maximum pollination efficiency, because in this self-pollinating species, each female flower requires a neighboring male flower to provide pollen.     

Genetic and environmental sources of covariance among internal reproductive traits in the yellow dung fly

Substantial inter- and intraspecific variation is found in reproductive traits, but the evolutionary implications of this variation remain unclear. One hypothesis is that natural selection favours female reproductive morphology that allows females to control mating and fertilization and that diverse male reproductive traits arise as counter adaptations to subvert this control. Such co-evolution predicts the establishment of genetic correlations between male and female reproductive traits that closely interact during mating. Therefore, we measured phenotypic and genetic correlations between male and female reproductive tract characteristics in the yellow dung fly, Scathophaga stercoraria (Diptera: Scathophagidae), using a nested half-sib breeding experiment. We found significant heritabilities for the size of most reproductive tract traits investigated in both females (spermathecae and their ducts, accessory glands and their ducts) and males (testis size but not sperm length). Within the sexes, phenotypic and genetic correlations were mostly nil or positive, suggesting functional integration of or condition-dependent investment in internal reproductive traits. Negative intrasexual genetic correlations, potentially suggestive of resource allocation trade-offs, were not evident. Intersexual genetic correlations were mostly positive, reflecting expected allometries between male and female morphologies. Most interestingly, testis size correlated positively with female accessory gland size and duct length, potentially indicative of a co-evolutionary arms race. We discuss these and alternative explanations for these patterns of genetic covariance.     

Genetic variation and evolutionary trade-offs for sexual and asexual reproductive modes in Allium vineale (Liliaceae)

Populations of Allium vineale commonly include individuals with very different allocation patterns to three modes of reproduction: sexual flowers, aerially produced asexual bulbils, and belowground asexual offsets. If selection is currently acting to maintain these different allocation patterns there must be a genetic basis for variation in allocation to these three reproductive modes. In addition, negative genetic correlations between reproductive traits would imply evolutionary trade-offs among reproductive strategies. We evaluated the heritability of these allocation patterns by growing 16 clones from a single population in the greenhouse at two levels of fertilization. Bulb mass and the mass and number of bulbils, offsets, and flowers were used as response variables, in addition to the proportion allocated to each reproductive mode. We found evidence of substantial heritable variation in allocation to sexual reproduction and in allocation within the two modes of asexual reproduction, indicating high sensitivity of these allocation patterns to natural selection. We also found evidence of strong negative genetic correlations between bulbil and flower traits, as well as between bulbil and offset traits, with one group of genotypes allocating greater resources to aerial asexual bulbils and the second group allocating more resources to belowground asexual offsets and aerial flowers. Phenotypic plasticity in allocation to above- vs. belowground asexual reproduction and sexual vs. asexual aerial reproduction was limited, indicating that plants are unlikely to change reproductive mode in response to nutrient availability. Together, then, we have demonstrated strong heritability for, and trade-offs in, the reproductive allocation patterns within this plant population.     

WATER STRESS ALTERS THE GENETIC ARCHITECTURE OF FUNCTIONAL TRAITS ASSOCIATED WITH DROUGHT ADAPTATION IN AVENA BARBATA

Environmental stress can alter genetic variation and covariation underlying functional traits, and thus affect adaptive evolution in response to natural selection. However, the genetic basis of functional traits is rarely examined in contrasting resource environments, and consequently, there is no consensus regarding whether environmental stress constrains or facilitates adaptive evolution. We tested whether resource availability affects genetic variation for and covariation among seven physiological traits and seven morphological/performance traits by growing the annual grass Avena barbata in dry and well-watered treatments. We found that differences in the overall genetic variance–covariance ( G ) matrix between environments were driven by physiological traits rather than morphology and performance traits. More physiological traits were heritable in the dry treatment than the well-watered treatment and many of the genetic correlations among physiological traits were environment dependent. In contrast, genetic variation and covariation among the morphological and performance traits did not differ across treatments. Furthermore, genetic correlations between physiology and performance were stronger in the dry treatment, which contributed to differences in the overall G -matrix. Our results therefore suggest that physiological adaptation would be constrained by low heritable variation in resource-rich environments, but facilitated by higher heritable variation and stronger genetic correlations with performance traits in resource-poor environments.     

The genetic architecture of sexual conflict: male harm and female resistance in Callosobruchus maculatus

Males harm females during mating in a range of species. This harm is thought to evolve because it is directly or indirectly beneficial to the male, despite being costly to his mate. The resulting sexually antagonistic selection can cause sexual arms races. For sexually antagonistic co-evolution to occur, there must be genetic variation for traits involved in female harming and susceptibility to harm, but even then intersexual genetic correlations could facilitate or impede sexual co-evolution. Male Callosobruchus maculatus harm their mates during copulation by damaging the female's reproductive tract. However, there have been no investigations of the genetic variation in damage or in female susceptibility to damage, nor has the genetic covariance between these characters been assessed. Here, we use a full-sib/half-sib breeding design to show that male damage is heritable, whereas female susceptibility to damage is much less so. There is also a substantial positive genetic correlation between the two, suggesting that selection favouring damaging males will increase the prevalence of susceptible females. We also provide evidence consistent with intralocus sexual conflict in this species.     

High and Dry: Drought Stress, Sex-Allocation Trade-offs, and Selection on Flower Size in the Alpine Wildflower Polemonium viscosum (Polemoniaceae)

Sex-allocation trade-offs may maintain variation in secondary sexual characteristics if such traits vary in their benefits or costs in association with different genders. In Polemonium viscosum, large flowers benefit both male and female aspects of reproduction. In this study, I explore how resource investment in flower size influences the cost of allocation to male and female function. Large flowers exact a water cost in P. viscosum under dry conditions. In an extreme drought in 1997, experimentally watered plants had higher survival and fecundity than controls. By comparing allocation patterns between plants dying from drought and survivors, I tested whether the demographic cost of large flowers increases with allocation to fecundity. Controls that died showed a positive relationship between flower size and fruit production, while survivors showed a negative relationship or trade-off. Watered plants showed no such trade-off. To test whether drought affects the relationship of corolla size to male function, I used leaf-water potential in 1998 to classify plants as stressed or unstressed. Corolla size showed positive correlations to pollen per flower regardless of drought stress. I conclude that under drought the demographic cost of producing large flowers is gender dependent, such that viability selection favors either small-flowered plants with female-biased reproduction or larger-flowered plants with male-biased reproduction.     

Consequences of hierarchical allocation for the evolution of life-history traits

Resource allocation within individuals may often be hierarchical, and this may have important effects on genetic correlations and on trait evolution. For example, organisms may divide energy between reproduction and somatic growth and then subdivide reproductive resources. Genetic variation in allocation to pathways early in such hierarchies (e.g., reproduction) can cause positive genetic correlations between traits that trade off (e.g., offspring size and number) because some individuals invest more resources in reproduction than others. We used quantitative-genetic models to explore the evolutionary implications of allocation hierarchies. Our results showed that when variation in allocation early in the hierarchy exceeds subsequent variation in allocation, genetic covariances and initial responses to selection do not reflect trade-offs occurring at later levels in the hierarchy. This general pattern was evident for many starting allocations and optima and for whether traits contributed multiplicatively or additively to fitness. Finally, artificial selection on a single trait revealed masked trade-offs when variation in early allocation was comparable to subsequent variation in allocation. This result confirms artificial selection as a powerful, but not foolproof, method of detecting trade-offs. Thus, allocation hierarchies can profoundly affect life-history evolution by causing traits to evolve in the opposite direction to that predicted by trade-offs.     

Phenotypic and genetic correlations among floral traits in two species of Thalictrum

The evolution of dioecy in plants is expected to be followed by sex-specific selection, leading to sexual dimorphism. The extent of the response to selection depends on the genetic covariance structure between traits both within and between the sexes. Here I describe an investigation to determine phenotypic and genetic correlations between reproductive traits within cryptically dioecious Thalictrum pubescens and within morphologically dioecious T. dioicum. Females of T. pubescens produce flowers having stamens and pistils, appearing hermaphroditic. Genetic correlations were estimated as family-mean correlations among paternal half-sib families. Positive phenotypic and genetic correlations between parts of the same reproductive organs, as the anther and filament of the stamen, indicate developmental associations between these traits in both species. Negative genetic correlations were detected between pistil number and size of reproductive organs in T. dioicum and showed the same direction, but not significance, in T. pubescens. There was a negative phenotypic correlation between the number of stamens and the number of pistils within female flowers of T. pubescens. Within T. pubescens, there was a positive genetic correlation between the number of stamens in males and the number of pistils in females, indicating that floral evolution in males and females may not be independent in this species.     

Quantitative trait loci for floral morphology in Arabidopsis thaliana

A central question in biology is how genes control the expression of quantitative variation. We used statistical methods to estimate genetic variation in eight Arabidopsis thaliana floral characters (fresh flower mass, petal length, petal width, sepal length, sepal width, long stamen length, short stamen length, and pistil length) in a cosmopolitan sample of 15 ecotypes. In addition, we used genome-wide quantitative trait locus (QTL) mapping to evaluate the genetic basis of variation in these same traits in the Landsberg erecta x Columbia recombinant inbred line population. There was significant genetic variation for all traits in both the sample of naturally occurring ecotypes and in the Ler x Col recombinant inbred line population. In addition, broad-sense genetic correlations among the traits were positive and high. A composite interval mapping (CIM) analysis detected 18 significant QTL affecting at least one floral character. Eleven QTL were associated with several floral traits, supporting either pleiotropy or tight linkage as major determinants of flower morphological integration. We propose several candidate genes that may underlie these QTL on the basis of positional information and functional arguments. Genome-wide QTL mapping is a promising tool for the discovery of candidate genes controlling morphological development, the detection of novel phenotypic effects for known genes, and in generating a more complete understanding of the genetic basis of floral development.     

Analytic and simulation models predicting positive genetic correlations between traits linked by trade-offs

Summary Using a two-loci multiplicative model of resource allocation, we show how the existence of several levels of resource allocation may affect the sign of the genetic correlations between traits linked by trade-offs. Positive genetic correlations between components of fitness affected by genetic trade-offs may result from different amounts of genetic variability at the pleiotropic loci determining the allocation of resources. Thus positive genetic correlations may be obtained in the absence both of environmental variation and of differences between individuals in resource acquisition. Nevertheless, positive correlations between all components of fitness at the same time cannot be obtained without variability in the acquisition of resources.     

Fertility variation in Pinus sylvestris: A TEST OF SEXUAL ALLOCATION THEORY

Sexual allocation theory assumes trade-offs and negative genetic correlations between male and female allocation in hermaphrodite plants. We tested this assumption by studying variation in male and female fertility in two experimental populations of Pinus sylvestris. In these populations, the genotypes have been vegetatively replicated, which allowed separation of the genetic and environmental components of variation. The genetic components of variation accounted for 36% of the total variation in pollen production in the two populations, and for 54% of cone production. As assumed by sexual allocation theory, the genetic correlation of pollen and cone production was negative in both populations (-0.59 and -0.15). However, positive environmental correlations between these traits (0.43 and 0.45) resulted in no phenotypic correlation in one population and a positive phenotypic correlation in the other.     

Genetic variation and covariation of aphid life-history traits across unrelated host plants

A central paradigm of life-history theory is the existence of resource mediated trade-offs among different traits that contribute to fitness, yet observations inconsistent with this tenet are not uncommon. We previously found a clonal population of the aphid Myzus persicae to exhibit positive genetic correlations among major components of fitness, resulting in strong heritable fitness differences on a common host. This raises the question of how this genetic variation is maintained. One hypothesis states that variation for resource acquisition on different hosts may override variation for allocation, predicting strong fitness differences within hosts as a rule, but changes in fitness hierarchies across hosts due to trade-offs. Therefore, we carried out a life-table experiment with 17 clones of M. persicae, reared on three unrelated host plants: radish, common lambsquarters and black nightshade. We estimated the broad-sense heritabilities of six life-history traits on each host, the genetic correlations among traits within hosts, and the genetic correlations among traits on different hosts (cross-environment genetic correlations). The three plants represented radically different environments with strong effects on performance of M. persicae, yet we detected little evidence for trade-offs. Fitness components were positively correlated within hosts but also between the two more benign hosts (radish and lambsquarters), as well as between those and another host tested earlier. The comparison with the most stressful host, nightshade, was hampered by low survival. Survival on nightshade also exhibited genetic variation but was unrelated to fitness on other hosts. Acknowledging that the number of environments was necessarily limited in a quantitative genetic experiment, we suggest that the rather consistent fitness hierarchies across very different plants provided little evidence to support the idea that the clonal variation for life-history traits and their covariance structure are maintained by strong genotypexenvironment interactions with respect to hosts. Alternative explanations are discussed.     

细枝柃性别表达特性及资源分配

已有的资料将柃木属(Eurya)描述为严格的雌雄异株植物, 性别变异现象极为少见。目前仅在柃木(E. japonica)和钝叶柃(E. obtusifolia)等少数种类中报道过两性花的存在。近几年笔者发现细枝柃(E. loquaiana)存在性别变异现象, 性别变异株上具有不同性别类型的花。该文从单花和植株水平分析了细枝柃的性别表达特性, 并对不同类型花的花部构件生物量分配进行比较分析。结果表明, 细枝柃具有6种类型的花, 从单花水平上看, 细枝柃性别有雌性、雄性及两性3种类型; 细枝柃性别在植株水平上体现较为复杂, 有雌株, 雄株, 雌花和两性花同株, 雄花和两性花同株, 雌雄异花同株及雌花、雄花、两性花同株6种类型; 在细枝柃花部构件生物量分配中, 雄花(包括雄株花和变异株雄花)花部构件生物量分配中雄蕊生物量的分配低于雌花(包括雌株花和变异株雌花)中雌蕊生物量的分配; 两性花中, 雄蕊生物量分配低于雌蕊, 这是其优化资源分配的手段, 进而获取最大适合度收益。     

Correlational selection and the evolution of genomic architecture

We review and discuss the importance of correlational selection (selection for optimal character combinations) in natural populations. If two or more traits subject to multivariate selection are heritable, correlational selection builds favourable genetic correlations through the formation of linkage disequilibrium at underlying loci governing the traits. However, linkage disequilibria built up by correlational selection are expected to decay rapidly (ie, within a few generations), unless correlational selection is strong and chronic. We argue that frequency-dependent biotic interactions that have 'Red Queen dynamics' (eg, host-parasite interactions, predator-prey relationships or intraspecific arms races) often fuel chronic correlational selection, which is strong enough to maintain adaptive genetic correlations of the kind we describe. We illustrate these processes and phenomena using empirical examples from various plant and animal systems, including our own recent work on the evolutionary dynamics of a heritable throat colour polymorphism in the side-blotched lizard Uta stansburiana. In particular, male and female colour morphs of side-blotched lizards cycle on five- and two-generation (year) timescales under the force of strong frequency-dependent selection. Each morph refines the other morph in a Red Queen dynamic. Strong correlational selection gradients among life history, immunological and morphological traits shape the genetic correlations of the side-blotched lizard polymorphism. We discuss the broader evolutionary consequences of the buildup of co-adapted trait complexes within species, such as the implications for speciation processes.     

Correlation between male and female reproduction in the subdioecious herb Astilbe biternata (Saxifragaceae)

Genotypic trade-offs between male and female reproduction are commonly assumed in theoretical studies of the evolution of gender specialization. Although these trade-offs are supported by higher seed production of females than hermaphrodites in natural populations of gynodioecious species, comparisons between male and female reproductive allocation among hermaphrodite individuals under controlled conditions are rare. We assessed phenotypic and genotypic correlations between stamen and fruit production in fruiting males of the near-dioecious herb Astilbe biternata. In the field, we found a significant negative phenotypic correlation between stamen production and fruit production within individuals that produced both stamens and fruit as well as higher fruit set in females than fruiting males. The negative correlation between fruit and stamen production that was observed in the field was also apparent across clonally propagated genotypes. These results suggest that negative genetic correlations between male and female reproduction may limit the independent evolution of fruit and stamen production in A. biternata.     

THE GENETIC BASIS OF THE TRADE-OFF BETWEEN CALLING AND WING MORPH IN MALES OF THE CRICKET GRYLLUS FIRMUS

Wing dimorphisms exist in a wide range of insects. In wing-dimorphic species one morph is winged has functional flight muscles (LW), and is flight-capable, whereas the other has reduced wings (SW) and cannot fly The evolution and maintenance of wing dimorphisms is believed to be due to trade-offs between flight capability and fitness-related traits. Although there are well-established phenotypic trade-offs associated with wing dimorphism in female insects, there only exist two studies that have established a genetic basis to these trade-offs. The present study provides the first evidence for a genetically based trade-off in male insects, specifically in the sand cricket Gryllus firmus. Because they have to expend energy to maintain the flight apparatus (especially flight muscles), LW males are predicted to call less and therefore to attract fewer females. To be of evolutionary significance, call duration wing morph, and wing muscle condition (size and functionality) should all have measurable heritabilities and all be genetically correlated. Differences between morphs in male G. firmus in the likelihood of attracting a female were tested in the laboratory using a T-maze where females chose between a LW male and a SW male. Call duration for each male was recorded on the sixth day of adult life. A significant difference in call duration was found between SW and LW males (SW = 0.86 ± 0.01, LW = 0.64 ± 0.01 h). SW males attracted significantly more females than did LW males (63% vs. to 37%). All the traits involved in the trade-off had significant heritabilities (call = 0 75 ± 0 33; wing morph = 0.22 ± 007; muscle weight = 0.38 ± 0.09) and genetic correlations (call and wing morph = -0.46 ± 0.20 for SW, -0.68 ± 0.16 for LW; LW call and muscle weight = -0.80 ± 0.14). These results provide the first documented evidence that trade-offs between a dimorphic trait and a fitness-related character in males has a genetic basis and hence can be of evolutionary significance.     

QUANTITATIVE GENETICS OF SEXUAL SELECTION IN THE FIELD CRICKET,GRYLLUS INTEGER

Major theories of sexual selection predict heritable variation in female preferences and male traits and a positive genetic correlation between preference and trait. Here we show that female Texas field crickets, Gryllus integer, have heritable genetic variation for the male calling song stimulus level that produces the greatest phonotactic response. Approximately 34% of the variation in female preferences was due to additive genetic effects. Female choosiness, that is, the strength of the female response to her most preferred stimulus relative to her average response to all stimuli, did not show significant genetic effects. The male calling song character was not related to male size or age but did show significant genetic effects. Approximately 39% of the variation in the number of pulses per trill was due to additive genetic variation. The genetic correlation estimated for the field population was 0.51 ± 0.17. The number of pulses per trill produced by males is under stabilizing sexual selection.