MULTI‐LEVEL SEXUAL SELECTION: INDIVIDUAL AND FAMILY‐LEVEL SELECTION FOR MATING SUCCESS IN A HISTORICAL HUMAN POPULATION

Precopulatory sexual selection is the association between fitness and traits associated with mate acquisition. Although sexual selection is generally recognized to be a powerful evolutionary force, most investigations are limited to characters belonging to individuals. A broader multilevel perspective acknowledges that individual fitness can be affected by aspects of mating success that are characters of groups, such as families. Parental mating success in polygynous or polyandrous human societies may exemplify traits under group‐level sexual selection. Using fitness measures that account for age‐structure, I measure multilevel selection for mate number over 55 years in a human population with declining rates of polygyny. Sexual selection had three components: individual‐level selection for ever‐mating (whether an individual mated) and individual‐ and family‐level selection for polyandry and polygyny. Family‐ and individual‐level selection for polygyny was equally strong, three times stronger than family‐level selection for polyandry and more than an order of magnitude stronger than individual‐level selection for polyandry. However, individual‐level selection for polyandry and polygyny was more effective at explaining relative fitness variance than family‐level selection. Selection for ever‐mating was the most important source of sexual selection for fitness; variation for ever‐mating explained 23% of relative fitness variance.     

THE COSTS AND BENEFITS OF TOLERANCE TO COMPETITION IN IPOMOEA PURPUREA,THE COMMON MORNING GLORY

Tolerance to competition has been hypothesized to reduce the negative impact of plant–plant competition on fitness. Although competitive interactions are a strong selective force, an analysis of net selection on tolerance to competition is absent in the literature. Using 55 full/half‐sibling families from 18 maternal lines in the crop weed Ipomoea purpurea, we measured fitness and putative tolerance traits when grown with and without competition in an agricultural field. We tested for the presence of genetic variation for tolerance to competition and determined if there were costs and benefits of this trait. We also assessed correlations between tolerance and potential tolerance traits. We uncovered a fitness benefit of tolerance in the presence of competition and a cost in its absence. We failed to detect evidence of additive genetic variation underlying tolerance, but did uncover the presence of a significant maternal‐line effect for tolerance, which suggests its evolutionary trajectory is not easily predicted. The cost of tolerance is likely due to later initiation of flowering of tolerant individuals in the absence of competition, whereas relative growth rate was found to positively covary with tolerance in the presence of competition, and can thus be considered a tolerance trait.     

GENOMIC BASIS OF AGING AND LIFE‐HISTORY EVOLUTION IN DROSOPHILA MELANOGASTER

Natural diversity in aging and other life‐history patterns is a hallmark of organismal variation. Related species, populations, and individuals within populations show genetically based variation in life span and other aspects of age‐related performance. Population differences are especially informative because these differences can be large relative to within‐population variation and because they occur in organisms with otherwise similar genomes. We used experimental evolution to produce populations divergent for life span and late‐age fertility and then used deep genome sequencing to detect sequence variants with nucleotide‐level resolution. Several genes and genome regions showed strong signatures of selection, and the same regions were implicated in independent comparisons, suggesting that the same alleles were selected in replicate lines. Genes related to oogenesis, immunity, and protein degradation were implicated as important modifiers of late‐life performance. Expression profiling and functional annotation narrowed the list of strong candidate genes to 38, most of which are novel candidates for regulating aging. Life span and early age fecundity were negatively correlated among populations; therefore, the alleles we identified also are candidate regulators of a major life‐history trade‐off. More generally, we argue that hitchhiking mapping can be a powerful tool for uncovering the molecular bases of quantitative genetic variation.     

THE RESPONSE TO SELECTION FOR FAST LARVAL DEVELOPMENT IN DROSOPHILA MELANOGASTER AND ITS EFFECT ON ADULT WEIGHT: AN EXAMPLE OF A FITNESS TRADE-OFF

A selection experiment using Drosophila melanogaster revealed a strong trade-off between adult weight and larval development time (LDT), supporting the view that antagonistic pleiotropy for these two fitness traits determines mean adult size. Two experimental lines of flies were selected for a shorter LDT (measured from egg laying to pupation). After 15 generations LDT was reduced by an average of 7.9%. The response appeared to be controlled primarily by autosomal loci. A correlated response to the selection was a reduction in adult dry weight: individuals from the selected populations were on average 15.1% lighter than the controls. The lighter females of the selected lines showed a 35% drop in fecundity, but no change in longevity. Thus, there is no direct relationship between LDT and adult longevity. The genetic correlation between weight and LDT, as measured from their joint response to selection, was 0.86. Although there was weak evidence for dominance in LDT, there was none for weight, making it unlikely that selection acting on this antagonistic pleiotropy could lead to a stable polymorphism. In all lines, sex differences in weight violated expectations based on intrasex genetic correlations: Females, being larger than males, ought to require a longer LDT, whereas there was a slight trend in the opposite direction. Because the sexual dimorphism in size was not significantly altered by selection, it appears that the controlling loci are either invariant or have very limited pleiotropic effect on developmental time. It is suggested that they probably control some intrinsic, energy-intensive developmental process in males.     

FLUCTUATING SELECTION AND THE MAINTENANCE OF INDIVIDUAL AND SEX‐SPECIFIC DIET SPECIALIZATION IN FREE‐LIVING OYSTERCATCHERS

Fluctuating and disruptive selection are important mechanisms for maintaining intrapopulation trait variation. Nonetheless, few field studies quantify selection pressures over long periods and identify what causes them to fluctuate. Diet specialists in oystercatchers differ in short‐term payoffs (intake), but their long‐term payoffs are hypothesized to be condition dependent. We test whether phenotypic selection on diet specialization fluctuates between years due to the frequency of specialists, competitor density, prey abundance, and environmental conditions. Short‐term payoffs proved to be poor predictors of long‐term fitness payoffs of specialization. Sex‐differences in diet specialization were maintained by opposing directional fecundity and viability selection between the sexes. Contrasting other studies, selection on individual diet specialization was neither negative frequency‐ or density‐dependent nor dependent on prey abundance. Notwithstanding, viability selection fluctuated strongly (stabilizing?disruptive) over the 26‐year study period: slightly favoring generalists in most years, but strongly disfavoring generalists in rare harsh winters, suggesting generalists cannot cope with extreme conditions. Although selection fluctuated, mean selection on specialists was weak, which can explain how individual specialization can persist over long periods. Because rare events can dramatically affect long‐term selective landscapes, more care should be taken to match the timescale of evolutionary studies to the temporal variability of critical environmental conditions.     

LIFE HISTORY VARIATION IN AN ARTIFICIALLY SELECTED POPULATION OF DROSOPHILA MELANOGASTER: PLEIOTROPY,SUPERFLIES, AND AGE‐SPECIFIC ADAPTATION

We measured age‐specific fecundity and survival in recombinant inbred lines of Drosophila melanogaster that were derived from an artificial selection experiment for delayed reproduction. Age at peak oviposition is highly heritable (h²_B= 0.55). We find three qualitative categories of peak oviposition: early‐, midlife‐, and bimodal. Genetic correlations between life span and early fecundity are not significantly different from zero, but correlations with midlife fecundity are positive and statistically significant. Long‐lived genotypes exhibit a midlife fecundity peak. There is no evidence for a shift of reproductive effort from early to later stages. The existence of qualitatively recombinant phenotypes, including “superflies” that exhibit both enhanced survival and high levels of early fecundity, argues against the widespread idea that life history evolution in Drosophila is dominated by negative pleiotropy. There is clear evidence of age‐specific adaptation in the timing of oviposition.     

SEXUAL SELECTION AND FITNESS VARIATION IN A POPULATION OF SMALLMOUTH BASS,MICROPTERUS DOLOMIEUI (PISCES: CENTRARCHIDAE)

Monogamy is often presumed to constrain mating variance and restrict the action of sexual selection. We examined the reproductive patterns of a monogamous population of smallmouth bass (Micropterus dolomieui), and attempted to identify sources of within-season fitness variation among females and known-age males. Many males did not acquire a nest site, and many territorial males were unsuccessful in acquiring a mate. The likelihood that territorial males mated depended on several aspects of nest sites. Mated males of age three were larger than the average size of age-three males in the population. The mean sizes of age-four and age-five mated males were not different from the average of same-age males in the population. Thus, selection resulting from the acquisition of a mate favored large size among only age-three males. Timing of nest construction and breeding among territorial males was negatively related to male size and did not depend on male age after taking male size into account. Indirect evidence (numbers of eggs deposited in nests) suggests that the timing of spawning among females was also negatively related to female size. Fertility selection favored early reproduction within the season by males of all ages, but large male size was favored among only age-four males. The combined early breeding of fecund females and female mate choice of large males may explain the positive correlation between the size of age-four males and the number of eggs acquired. Despite large differences of female fecundity, however, the variance of relative mate number contributed about two times more than the variance of relative fertility among females to the total variance of relative fitness within each sex.     

SIZE‐FECUNDITY RELATIONSHIPS,GROWTH TRAJECTORIES,AND THE TEMPERATURE‐SIZE RULE FOR ECTOTHERMS

Many ectotherms show crossing growth trajectories as a plastic response to rearing temperature. As a result, individuals growing up in cool conditions grow slower, mature later, but are larger at maturation than those growing up in warm conditions. To date, no entirely satisfactory explanation has been found for why this pattern, often called the temperature‐size rule, should exist. Previous theoretical models have assumed that size‐specific mortality rates were most likely to drive the pattern. Here, I extend one theoretical model to show that variation in size‐fecundity relationships may also be important. Plasticity in the size‐fecundity relationship has rarely been considered, but a number of studies show that fecundity increases more quickly with size in cold environments than it does in warm environments. The greater increase in fecundity offsets costs of delayed maturation in cold environments, favoring a larger size at maturation. This can explain many cases of crossing growth trajectories, not just in relation to temperature.     

TRAIT COMPENSATION AND SEX‐SPECIFIC AGING OF PERFORMANCE IN MALE AND FEMALE PROFESSIONAL BASKETBALL PLAYERS

Phenotypic traits are often influenced by dynamic resource allocation trade‐offs which, when occurring over the course of individual lifespan, may manifest as trait aging. Although aging is studied for a variety of traits that are closely tied to reproduction or reproductive effort, the aging of multiple traits related to fitness in other ways are less well understood. We took advantage of almost 30 years of data on human whole‐organism performance in the National Basketball Association (USA) to examine trends of aging in performance traits associated with scoring. Given that patterns of aging differ between sexes in other animal species, we also analyzed a smaller dataset on players in the Women's National Basketball Association to test for potential sex differences in the aging of comparable traits. We tested the hypothesis that age‐related changes in a specific aspect of overall performance can be compensated for by elevated expression of another, related aspect. Our analyses suggest that the aging of performance traits used in basketball is generally characterized by senescence in males, whereas age‐related changes in basketball performance are less evident in females. Our data also indicate a different rate of senescence of different performance traits associated with scoring over a male's lifetime.     

THE INTENSITY OF SELECTION ACTING ON THE COUCH POTATO GENE—SPATIAL–TEMPORAL VARIATION IN A DIAPAUSE CLINE

Cosmopolitan populations of Drosophila melanogaster have co‐opted a form of reproductive diapause to overwinter in northern populations. Polymorphism in the couch potato gene has been implicated in genetic variation for this diapause trait. Using a collection of 20 populations from Florida to Canada and 11 collections from 3 years in a Pennsylvania orchard, we estimated the allele frequencies for 15 single nucleotide polymorphisms (SNPs) in the couch potato gene. These include the specific polymorphism associated with diapause inducability. We find that the SNP polymorphism, 48034(A/T), is correlated with latitude and its frequencies are predicted by the incidence of diapause trait. We find that the clinal patterns for cpo SNPs sampled in 1997 are similar to the same SNPs sampled in 2009–2010. SNPs that show apparent associations with cpo expression are also clinal with the low‐expression allele increasing in frequency, as would be predicted from functional knockout studies of cpo. Finally, we see a significant pattern where the frequency of the diapause‐causing allele drops in frequency during the summer season, consistent with the drop in the incidence of the diapause trait. The selection required to drive this response is large, roughly 24% to 59% per generation depending on the degree of dominance.     

GENE FLOW AND SELECTION ON PHENOTYPIC PLASTICITY IN AN ISLAND SYSTEM OF RANA TEMPORARIA

Gene flow is often considered to be one of the main factors that constrains local adaptation in a heterogeneous environment. However, gene flow may also lead to the evolution of phenotypic plasticity. We investigated the effect of gene flow on local adaptation and phenotypic plasticity in development time in island populations of the common frog Rana temporaria which breed in pools that differ in drying regimes. This was done by investigating associations between traits (measured in a common garden experiment) and selective factors (pool drying regimes and gene flow from other populations inhabiting different environments) by regression analyses and by comparing pairwise F_ST values (obtained from microsatellite analyses) with pairwise Q_ST values. We found that the degree of phenotypic plasticity was positively correlated with gene flow from other populations inhabiting different environments (among‐island environmental heterogeneity), as well as with local environmental heterogeneity within each population. Furthermore, local adaptation, manifested in the correlation between development time and the degree of pool drying on the islands, appears to have been caused by divergent selection pressures. The local adaptation in development time and phenotypic plasticity is quite remarkable, because the populations are young (less than 300 generations) and substantial gene flow is present among islands.     

PRODUCTIVITY AND DIVERSITY IN A CROSS‐FEEDING POPULATION OF ARTIFICIAL ORGANISMS

Cross‐feeding interactions are a common feature of many microbial systems, such as colonies of Escherichia coli grown on a single limiting resource, and microbial consortia cooperatively degrading complex compounds. We have studied this phenomenon from an abstract point of view by considering artificial organisms that metabolize binary strings from a shared environment. The organisms are represented as simple cellular automaton rules and the analog of energy in the system is an approximation of the Shannon entropy of the binary strings. Only organisms that increase the entropy of the transformed strings are allowed to replicate. This system exhibits a large degree of species diversity, which increases when the flow of binary strings into the system is reduced. Investigating the relation between ecosystem productivity and diversity we find that diversity is negatively correlated with biomass production and energy uptake, while it correlates positively with energy‐uptake efficiency. By performing invasion experiments, we show that the source of diversity is negative frequency‐dependent selection acting among the different species, and that some of these interactions are intransitive, another mechanism known to promote diversity.     

THE MAINTENANCE OF GENETIC VARIATION FOR OVIPOSITION RATE IN TWO‐SPOTTED SPIDER MITES: INFERENCES FROM ARTIFICIAL SELECTION

Despite the directional selection acting on life‐history traits, substantial amounts of standing variation for these traits have frequently been found. This variation may result from balancing selection (e.g., through genetic trade‐offs) or from mutation‐selection balance. These mechanisms affect allele frequencies in different ways: Under balancing selection alleles are maintained at intermediate frequencies, whereas under mutation‐selection balance variation is generated by deleterious mutations and removed by directional selection, which leads to asymmetry in the distribution of allele frequencies. To investigate the importance of these two mechanisms in maintaining heritable variation in oviposition rate of the two‐spotted spider mite, we analyzed the response to artificial selection. In three replicate experiments, we selected for higher and lower oviposition rate, compared to control lines. A response to selection only occurred in the downward direction. Selection for lower oviposition rate did not lead to an increase in any other component of fitness, but led to a decline in female juvenile survival. The results suggest standing variation for oviposition rate in this population consists largely of deleterious alleles, as in a mutation‐selection balance. Consequently, the standing variation for this trait does not appear to be indicative of its adaptive potential.     

RECONSTRUCTING ORIGINS OF LOSS OF SELF‐INCOMPATIBILITY AND SELFING IN NORTH AMERICAN ARABIDOPSIS LYRATA: A POPULATION GENETIC CONTEXT

Theoretical and empirical comparisons of molecular diversity in selfing and outcrossing plants have primarily focused on long‐term consequences of differences in mating system (between species). However, improving our understanding of the causes of mating system evolution requires ecological and genetic studies of the early stages of mating system transition. Here, we examine nuclear and chloroplast DNA sequences and microsatellite variation in a large sample of populations of Arabidopsis lyrata from the Great Lakes region of Eastern North American that show intra‐ and interpopulation variation in the degree of self‐incompatibility and realized outcrossing rates. Populations show strong geographic clustering irrespective of mating system, suggesting that selfing either evolved multiple times or has spread to multiple genetic backgrounds. Diversity is reduced in selfing populations, but not to the extent of the severe loss of variation expected if selfing evolved due to selection for reproductive assurance in connection with strong founder events. The spread of self‐compatibility in this region may have been favored as colonization bottlenecks following glaciation or migration from Europe reduced standing levels of inbreeding depression. However, our results do not suggest a single transition to selfing in this system, as has been suggested for some other species in the Brassicaceae.     

GENETICS OF INCIPIENT SPECIATION IN DROSOPHILA MOJAVENSIS. III. LIFE‐HISTORY DIVERGENCE IN ALLOPATRY AND REPRODUCTIVE ISOLATION

We carried out a three‐tiered genetic analysis of egg‐to‐adult development time and viability in ancestral and derived populations of cactophilic Drosophila mojavensis to test the hypothesis that evolution of these life‐history characters has shaped premating reproductive isolation in this species. First, a common garden experiment with 11 populations from Baja California and mainland Mexico and Arizona reared on two host species revealed significant host plant X region and population interactions for viability and development time, evidence for host plant adaptation. Second, replicated line crosses with flies reared on both hosts revealed autosomal, X chromosome, cytoplasmic, and autosome X cactus influences on development time. Viability differences were influenced by host plants, autosomal dominance, and X chromosomal effects. Many of the F₁, F₂, and backcross generations showed evidence of heterosis for viability. Third, a QTL analysis of male courtship song and epicuticular hydrocarbon variation based on 1688 Baja × mainland F₂ males also revealed eight QTL influencing development time differences. Mainland alleles at six of these loci were associated with longer development times, consistent with population‐level differences. Eight G × E interactions were also detected caused by longer development times of mainland alleles expressed on a mainland host with smaller differences among Baja genotypes reared on the Baja host plant. Four QTL influenced both development time and epicuticular hydrocarbon differences associated with courtship success, and there was a significant QTL‐based correlation between development time and cuticular hydrocarbon variation. Thus, the regional shifts in life histories that evolved once D. mojavensis invaded mainland Mexico from Baja California by shifting host plants were genetically correlated with variation in cuticular hydrocarbon‐based mate preferences.     

EVOLUTION OF VIVIPARITY: A PHYLOGENETIC TEST OF THE COLD‐CLIMATE HYPOTHESIS IN PHRYNOSOMATID LIZARDS

The evolution of viviparity is a key life‐history transition in vertebrates, but the selective forces favoring its evolution are not fully understood. With >100 origins of viviparity, squamate reptiles (lizards and snakes) are ideal for addressing this issue. Some evidence from field and laboratory studies supports the “cold‐climate” hypothesis, wherein viviparity provides an advantage in cold environments by allowing mothers to maintain higher temperatures for developing embryos. Surprisingly, the cold‐climate hypothesis has not been tested using both climatic data and phylogenetic comparative methods. Here, we investigate the evolution of viviparity in the lizard family Phrynosomatidae using GIS‐based environmental data, an extensive phylogeny (117 species), and recently developed comparative methods. We find significant relationships between viviparity and lower temperatures during the warmest (egg‐laying) season, strongly supporting the cold‐climate hypothesis. Remarkably, we also find that viviparity tends to evolve more frequently at tropical latitudes, despite its association with cooler climates. Our results help explain this and two related patterns that seemingly contradict the cold‐climate hypothesis: the presence of viviparous species restricted to low‐elevation tropical regions and the paucity of viviparous species at high latitudes. Finally, we examine whether viviparous taxa may be at higher risk of extinction from anthropogenic climate change.     

THE ROLES OF LIFE‐HISTORY SELECTION AND SEXUAL SELECTION IN THE ADAPTIVE EVOLUTION OF MATING BEHAVIOR IN A BEETLE

Although there is continuing debate about whether sexual selection promotes or impedes adaptation to novel environments, the role of mating behavior in such adaptation remains largely unexplored. We investigated the evolution of mating behavior (latency to mating, mating probability and duration) in replicate populations of seed beetles Callosobruchus maculatus subjected to selection on life‐history (“Young” vs. “Old” reproduction) under contrasting regimes of sexual selection (“Monogamy” vs. “Polygamy”). Life‐history selection is predicted to favor delayed mating in “Old” females, but sexual conflict under polygamy can potentially retard adaptive life‐history evolution. We found that life‐history selection yielded the predicted changes in mating behavior, but sexual selection regime had no net effect. In within‐line crosses, populations selected for late reproduction showed equally reduced early‐life mating probability regardless of mating system. In between‐line crosses, however, the effect of life‐history selection on early‐life mating probability was stronger in polygamous lines than in monogamous ones. Thus, although mating system influenced male–female coevolution, removal of sexual selection did not affect the adaptive evolution of mating behavior. Importantly, our study shows that the interaction between sexual selection and life‐history selection can result in either increased or decreased reproductive divergence depending on the ecological context.     

TRADE‐OFFS,SPATIAL HETEROGENEITY,AND THE MAINTENANCE OF MICROBIAL DIVERSITY

Specialization and concomitant trade‐offs are assumed to underlie the non‐neutral coexistence of lineages. Trade‐offs across heterogeneous environments can promote diversity by preventing competitive exclusion. However, the importance of trade‐offs in maintaining diversity in natural microbial assemblages is unclear, as trade‐offs are frequently not detected in artificial evolution experiments. Stressful conditions associated with patches of heavy‐metal enriched serpentine soils provide excellent opportunities for examining how heterogeneity may foster genetic diversity. Using a spatially replicated design, we demonstrate that rhizobium bacteria symbiotic with legumes inhabiting contrasting serpentine and nonserpentine soils exhibit a trade‐off between a genotype's nickel tolerance and its ability to replicate rapidly. Furthermore, we detected adaptive divergence in rhizobial assemblages across soil type heterogeneity at multiple sites, suggesting that this trade‐off may promote the coexistence of phenotypically distinct bacterial lineages. Trade‐offs and adaptive divergence may be important factors maintaining the tremendous diversity within natural assemblages of bacteria.