Direct Targets Of Selection Research Articles

EVOLUTION OF VARIATION AND VARIABILITY UNDER FLUCTUATING, STABILIZING, AND DISRUPTIVE SELECTION

How variation and variability (the capacity to vary) may respond to selection remain open questions. Indeed, effects of different selection regimes on variational properties, such as canalization and developmental stability are under debate. We analyzed the patterns of among- and within-individual variation in two wing-shape characters in populations of Drosophila melanogaster maintained under fluctuating, disruptive, and stabilizing selection for more than 20 generations. Patterns of variation in wing size, which was not a direct target of selection, were also analyzed. Disruptive selection dramatically increased phenotypic variation in the two shape characters, but left phenotypic variation in wing size unaltered. Fluctuating and stabilizing selection consistently decreased phenotypic variation in all traits. In contrast, within-individual variation, measured by the level of fluctuating asymmetry, increased for all traits under all selection regimes. These results suggest that canalization and developmental stability are evolvable and presumably controlled by different underlying genetic mechanisms, but the evolutionary responses are not consistent with an adaptive response to selection on variation. Selection also affected patterns of directional asymmetry, although inconsistently across traits and treatments.

ASYMMETRY OF GENETIC VARIATION IN FITNESS-RELATED TRAITS: APPARENT STABILIZING SELECTION ONgmax

The maintenance of genetic variation in traits closely associated with fitness remains a key unresolved issue in evolutionary genetics. One important qualification on the observation of genetic variation in fitness-related traits is that such traits respond asymmetrically to selection, evolving to a greater extent in the direction of lower fitness. Here we test the hypothesis that standing genetic variation in fitness-related traits is principally maintained for unfit phenotypes. Male Drosophila bunnanda vary in mating success (the primary determinant of male fitness) due to female mate choice. We used competitive mating success to partitioning males into two groups: successful (high fitness) and unsuccessful (low fitness). Relative to successful males, unsuccessful males harbored considerably greater levels of additive genetic variation for sexual signaling traits. This genetic asymmetry was detected for a multivariate trait that we demonstrated was not directly under stabilizing sexual selection, leading us to conclude the trait was under apparent stabilizing selection. Consequently, our results suggest genetic variance might be biased toward low fitness even for traits that are not themselves the direct targets of selection. Simple metrics of genetic variance are unlikely to be adequate descriptors of the complex nature of the genetic basis of traits under selection.

The fitness advantage of a high-performance weapon

Weapons used in combat between males are usually attributed to sexual selection, which operates via a fitness advantage for males with weapons of better ‘quality’. Because the performance capacity of morphological traits is typically considered the direct target of selection, Darwin’s intrasexual selection hypothesis can be modified to predict that variation in reproductive success should be explained by variation in performance traits relevant to combat. Despite such a straightforward prediction, tests of this hypothesis are conspicuously lacking. We show that territorial male collared lizards with greater bite-force capacity sire more offspring than weaker biting rivals but exhibit no survival advantage. We did not detect stabilizing or disruptive selection on bite-force capacity. Taken together, these results support the hypothesis that superior weapon performance provides a fitness advantage through increased success in male contests. Sexual selection on weapon performance therefore appears to be a force driving the evolution and maintenance of sexual dimorphism in head shape. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 840‐845.

Enhanced ectodysplasin-A receptor (EDAR) signaling alters multiple fiber characteristics to produce the East Asian hair form

Hair morphology differs dramatically between human populations: people of East Asian ancestry typically have a coarse hair texture, with individual fibers being straight, of large diameter, and cylindrical when compared to hair of European or African origin. Ectodysplasin-A receptor (EDAR) is a cell surface receptor of the tumor necrosis factor receptor (TNFR) family involved in the development of hair follicles, teeth, and sweat glands. Analyses of genome-wide polymorphism data from multiple human populations suggest that EDAR experienced strong positive selection in East Asians. It is likely that a nonsynonymous SNP in EDAR, rs3827760, was the direct target of selection as the derived p.Val370Ala variant is seen at high frequencies in populations of East Asian and Native American origin but is essentially absent from European and African populations. Here we demonstrate that the derived EDAR370A common in East Asia has a more potent signaling output than the ancestral EDAR370 V in vitro. We show that elevation of Edar activity in transgenic mice converts their hair phenotype to the typical East Asian morphology. The coat texture becomes coarse, with straightening and thickening of individual hairs and conversion of fiber cross-sectional profile to a circular form. These thick hair fibers are produced by enlarged hair follicles, which in turn develop from enlarged embryonic organ primordia. This work shows that the multiple differences in hair form between East Asian and other human populations can be explained by the simplest of genetic alterations.

Rampant Adaptive Evolution in Regions of Proteins with Unknown Function in Drosophila simulans

Adaptive protein evolution is pervasive in Drosophila. Genomic studies, thus far, have analyzed each protein as a single entity. However, the targets of adaptive events may be localized to particular parts of proteins, such as protein domains or regions involved in protein folding. We compared the population genetic mechanisms driving sequence polymorphism and divergence in defined protein domains and non-domain regions. Interestingly, we find that non-domain regions of proteins are more frequent targets of directional selection. Protein domains are also evolving under directional selection, but appear to be under stronger purifying selection than non-domain regions. Non-domain regions of proteins clearly play a major role in adaptive protein evolution on a genomic scale and merit future investigations of their functional properties.

Paternal alleles enhance female reproductive success in tropical pythons

The conventional view that female reproductive success is unlikely to benefit from multiple mating has come under strong challenge in recent years. In the present study, we demonstrate that the time wild-caught reproductive female water pythons (Liasis fuscus) spent in the laboratory prior to oviposition affected both hatching success and the number of male microsatellite alleles detected in the broods. A negative correlation between time in captivity and number of male alleles observed in the broods suggests that reduced hatching success was most likely not caused by environmental factors such as non-optimal temperatures, but rather by restricted mating opportunities. Maternal nutritional status and mean hatchling mass did not affect brood viability. However, our results revealed a positive correlation between number of male microsatellite alleles observed in the broods and hatching success, suggesting that increased paternal genetic variability enhanced female reproductive success. As microsatellite loci are unlikely to be direct targets of selection, we suggest that variability at these loci may cosegregate with other polymorphic genes directly linked to fitness.

Microclinal variation for ovariole number and body size in Drosophila melanogaster in ?Evolution Canyon?

Sites that display strong environmental contrasts in close proximity, such as 'Evolution Canyon' on Mt. Carmel, Israel, are natural theatres for investigating adaptive evolution in action. We reared Drosophila melanogaster from collection sites along altitudinal transects on the north- and south-facing canyon slopes in each of three temperature environments, and assessed genetic variation in ovariole number and body size between and within collection sites, and temperature plasticity. Both traits exhibited significant genetic variation within collection sites and phenotypic plasticity in response to temperature, but not genetic variation for plasticity. Between-site genetic variation in ovariole number was negatively correlated with altitude on both slopes of the canyon, and collections from the north- and south-facing slopes were genetically differentiated for male, but not female, body size. Genetic variation between sites within easy dispersal range is consistent with the action of strong natural selection, although neither the selective agent(s) nor the direct targets of selection are known.

Mosaic microecological differential stress causes adaptive microsatellite divergence in wild barley, Hordeum spontaneum, at Neve Yaar, Israel.

Genetic diversity at 38 microsatellite (short sequence repeats (SSRs)) loci was studied in a sample of 54 plants representing a natural population of wild barley, Hordeum spontaneum, at the Neve Yaar microsite in Israel. Wild barley at the microsite was organized in a mosaic pattern over an area of 3180 m2 in the open Tabor oak forest, which was subdivided into four microniches: (i) sun-rock (11 genotypes), (ii) sun-soil (18 genotypes), (iii) shade-soil (11 genotypes), and (iv) shade-rock (14 genotypes). Fifty-four genotypes were tested for ecological-genetic microniche correlates. Analysis of 36 loci showed that allele distributions at SSR loci were nonrandom but structured by ecological stresses (climatic and edaphic). Sixteen (45.7%) of 35 polymorphic loci varied significantly (p < 0.05) in allele frequencies among the microniches. Significant genetic divergence and diversity were found among the four subpopulations. The soil and shade subpopulations showed higher genetic diversities at SSR loci than the rock and sun subpopulations, and the lowest genetic diversity was observed in the sun-rock subpopulation, in contrast with the previous allozyme and RAPD studies. On average, of 36 loci, 88.75% of the total genetic diversity exists within the four microniches, while 11.25% exists between the microniches. In a permutation test, G(ST) was lower for 4999 out of 5000 randomized data sets (p < 0.001) when compared with real data (0.1125). The highest genetic distance was between shade-soil and sun-rock (D = 0.222). Our results suggest that diversifying natural selection may act upon some regulatory regions, resulting in adaptive SSR divergence. Fixation of some loci (GMS61, GMS1, and EBMAC824) at a specific microniche seems to suggest directional selection. The pattern of other SSR loci suggests the operation of balancing selection. SSRs may be either direct targets of selection or markers of selected haplotypes (selective sweep).

The functions of freezing in the social interactions of juvenile high‐ and low‐aggressive mice

AbstractSelectively bred low‐aggressive mice are frequently observed to freeze on social contact, despite the fact that this behavior was never a direct target of selection. To elucidate this finding, the present research aimed to identify the possible functions freezing may serve in social interactions. It was hypothesized that freezing may modify social interactions through self‐regulatory mechanisms and/or via its modulating effects on the actions of social partners. These hypotheses were evaluated with respect to the sequential changes observed over the course of a 10‐min dyadic test in freezing, social reactivity, and approaches among juvenile (24–30‐day‐old) mice from the NC900 and NC100 high‐ and low‐aggressive lines. Analyses of the patterns of social interactions between subjects and partners revealed two primary results. First, freezing was more than an expression of fear; it also functioned as a regulator of emotional arousal, as suggested by the substantial reduction of reactive behaviors seen in animals that showed high levels of freezing. Second, freezing functioned to facilitate high levels of affiliative social interaction with social partners. The implications of these results for understanding how the differentiation of the NC900 and NC100 occurred within microevolution and development are discussed. Aggr. Behav. 27:463–475, 2001. © 2001 Wiley‐Liss, Inc.

ABSOLUTE VERSUS RELATIVE MEASUREMENTS OF SEXUAL SELECTION: ASSESSING THE CONTRIBUTIONS OF ULTRASONIC SIGNAL CHARACTERS TO MATE ATTRACTION IN LESSER WAX MOTHS, ACHROIA GRISELLA (LEPIDOPTERA: PYRALIDAE).

When females choose a mate among a group of signaling males concentrated in a small area, a male's mating success is often determined not only by his absolute attractiveness but by the attractiveness of his neighbors as well. Multivariate analyses of sexual selection measurements based on absolute values of predictor variables are then misleading, because such analyses assume that the fitness of a given individual is not influenced by others. We addressed this problem of relative fitness in sexual selection by developing two adjustments of the predictor variables in the multivariate analyses by including group means in addition to absolute values and by using relative values, deviations from group means. In the lesser wax moth, Achroia grisella (Lepidoptera: Pyralidae), aggregated males produce ultrasonic signals attractive to females in the vicinity of honey bee colonies. Playback experiments showed that females prefer signals whose pulses are louder, longer, delivered at a faster rate, and include lengthy silent gaps within pulse pairs (long asynchrony intervals). To measure sexual selection on ultrasonic signals, attractiveness was assessed by observing the number of females orienting toward given males in four-choice trials. The various signal characters of the males were computed from ultrasound recordings. Multivariate regression and nonparametric analyses revealed that peak amplitude, asynchrony interval, and pulse rate were the direct targets of selection. Nonlinear stabilizing and correlational selection were also detected. Comparisons of results from multivariate analyses based on absolute values and on the two relative adjustments indicated that the quality of a four-male group did not affect the strength or direction of linear selection but changed the strength of nonlinear selection. Both relative adjustments improved the prediction of male attractiveness. Three-dimensional surface plots generated by the nonparametric regression analyses showed that attractiveness increased monotonically with any combination of the signal characters. This graphical technique also showed that female choice in A. grisella was based on a relative, as opposed to a threshold, decision rule. Overall, male attractiveness for the population remained consistent between testing days. However, attractiveness values for some individual males changed between successive testing days. In these cases, the change in attractiveness was related only to the change in peak amplitude.

BALANCING SELECTION IN A DESERT STREAM-DWELLING FISH, POECILIOPSIS MONACHA.

The desert stream-dwelling fish Poeciliopsis monacha is exposed to extreme seasonal and spatial variation in physical stresses. We examined four diallelic gene loci (Ldh-1, Idh-2, Pgd, and Ck-A) in P. monacha and tested whether genotypes were associated with differential survival of individuals exposed to acute stress. For each locus, the common allele was associated with higher survival during heat and hypoxic stress, whereas the alternate allele was associated with higher survival during cold stress. In most cases, survival of heterozygotes was intermediate and they exhibited less variance in survival than corresponding homozygotes. Identification of substantial linkage disequilibrium in these fish confounds our ability to discern whether the allozymes are the direct targets of selection, or if they just mark chromosomal regions that contain the true modifiers of survival. Nevertheless, the present results clearly identified balancing processes that can serve to stabilize genetic polymorphism in this species.

Sexual Selection and Sexual Dimorphism in the Harlequin Beetle Acrocinus longimanus

To investigate the causes of striking sexual dimorphism in the harlequin beetle (Acrocinus longimanus), we carried out a study of the behavior and morphology of two widely separated populations (in French Guiana and Panama). Males of this species possess greatly elongated forelegs which exhibit strong positive allometry with body size (elytra length). Males use their forelegs in fights with other males and in guarding females and oviposition sites. Field data on fighting and mating success suggest that sexual selection favors large size in males. However, the direct targets of selection were masked by high correlations between traits of the elytra, forelegs, and antennae. Sexual selection appears to be driven by intense male competition to monopolize suitable sites for egg deposition. Female harlequin beetles are highly selective in choosing only recently dead or dying trees for oviposition (Moraceae and Apocynaceae). Despite marked geographic variation in coloration, host trees, and climate, the two populations did not differ in mean size and extent of sexual dimorphism. We suggest that sexual selection in this species is sufficiently intense to override any effects of differing ecological factors.

EXAMINING HYPOTHESES GENERATED BY FIELD MEASURES OF SEXUAL SELECTION ON MALE LIZARDS, UTA PALMERI.

I examined sexual selection in the iguanid lizard Uta palmeri by measuring phenotypic selection in a cohort of males. Relative fitness was estimated by copulation rate from one breeding season, and I analyzed selection on five morphological traits (snout-vent length, mass, jaw length, head width, and head depth) and on male territory quality. Only territory quality and head depth were identified as direct targets of selection in a linear selection gradient analysis. Head depth was suggested to also be subject to quadratic selection. All traits exhibited significant directional selection differentials, suggesting indirect selection also was present because of the correlation of these traits with direct targets of selection. I used these results to generate hypotheses about the mechanisms of selection. For traits not identified as direct targets of selection (snout-vent length, mass, head width, jaw length), I could accept the null hypothesis of no female preference for the analyzed male traits; if these morphological traits were preferred by females in mate choice, they would have been identified as direct targets of selection. Exploring possible functional relationships within the cohort, I found that all five morphological traits contributed to explaining variation in territorial status. And in staged aggressive interactions between males that were similar in snout-vent length and mass, winning was associated only with greater head depth and not with head width or jaw length. Several possible interpretations of these results are presented. This study suggests that differential mating success arising from variation in territory quality gives rise to indirect selection on morphology. The possible mechanisms giving rise to the proposed direct selection on head depth require further study.