SOCIAL CAUSES OF CORRELATIONAL SELECTION AND THE RESOLUTION OF A HERITABLE THROAT COLOR POLYMORPHISM IN A LIZARD

Abstract When selection acts on social or behavioral traits, the fitness of an individual depends on the phenotypes of its competitors. Here, we describe methods and statistical inference for measuring natural selection in small social groups. We measured selection on throat color alleles that arises from microgeographic variation in allele frequency at natal sites of side‐blotched lizards (Uta stansburiana). Previous game‐theoretic analysis indicates that two color morphs of female side‐blotched lizards are engaged in an offspring quantity‐quality game that promotes a density‐and frequency‐dependent cycle. Orange‐throated females are r‐strategists. They lay large clutches of small progeny, which have poor survival at high density, but good survival at low density. In contrast, yellow‐throated females are K‐strategists. They lay small clutches of large progeny, which have good survival at high density. We tested three predictions of the female game: (1) orange progeny should have a fitness advantage at low density; (2) correlational selection acts to couple color alleles and progeny size; and (3) this correlational selection arises from frequency‐dependent selection in which large hatchling size confers an advantage, but only when yellow alleles are rare. We also confirmed the heritability of color, and therefore its genetic basis, by producing progeny from controlled matings. A parsimonious cause of the high heritability is that three alleles (o, b, y) segregate as one genetic factor. We review the physiology of color formation to explain the possible genetic architecture of the throat color trait. Heritability of color was nearly additive in our breeding study, allowing us to compute a genotypic value for each individual and thus predict the frequency of progeny alleles released on 116 plots. Rather than study the fitness of individual progeny, we studied how the fitness of their color alleles varied with allele frequency on plots. We confirmed prediction 1: When orange alleles are present in female progeny, they have higher fitness at low density when compared to other alleles. Even though the difference in egg size of the female morphs was small (0.02 g), it led to knife‐edged survival effects for their progeny depending on local social context. Selection on hatchling survival was not only dependent on color alleles, but on a fitness interaction between color alleles and hatchling size, which confirmed prediction 2. Sire effects, which are not confounded by maternal phenotype, allowed us to resolve the frequency dependence of correlational selection on egg size and color alleles and thereby confirmed prediction 3. Selection favored large size when yellow sire alleles were rare, but small size when they were common. Correlational selection promotes the formation of a self‐reinforcing genetic correlation between the morphs and life‐history variation, which causes selection in the next density and frequency cycle to be exacerbated. We discuss general conditions for the evolution of self‐reinforcing genetic correlations that arise from social selection associated with frequency‐dependent sexual and natural selection.     

Mate Preference for Novel Phenotypes: A Fresh Face Matters

Conspicuous polymorphism in sexually selected traits is usually attributed to processes such as frequency‐dependent selection that can maintain genetic variation. Recent evidence indicates that dramatic variation of male coloration in guppies (Poecilia reticulata) is promoted by a form of frequency‐dependent selection in which males bearing rare or novel color patterns achieve higher mating success than males bearing common patterns. Active female preference for unfamiliar or rare color patterns has been implicated in generating this rare‐phenotype advantage, but the behavioral processes responsible for the preference remain unclear. To determine whether familiarity that is developed over a very short timescale can lead to a rare‐male mating advantage, we measured female response to courtship by males with color patterns that were the same as or different from that of the previous male to court. Females showed two types of short‐term preference variation in this experiment. On the first trial day, females shifted their preferences on a timescale of minutes, showing strong preference for males bearing a color pattern different from that of the immediately previous male to court. Twenty‐four hours later, females were less responsive to male courtship overall, and there was no difference in females’ response to different‐ and same‐morph males. Females also preferred males with more orange coloration on both trial days, but this color preference was independent of the preference for ‘different’ color patterns. These data suggest that the behavioral process underlying rare‐male advantage in guppies is that females prefer males bearing unfamiliar color patterns and that familiarity is determined over a very short timescale.     

Predation Cost of Conspicuous Male Coloration in Collared Lizards (Crotaphytus collaris): An Experimental Test Using Clay-Covered Model Lizards

Animal color patterns are a compromise between sexual selection pressures that increase advantages accrued from conspicuousness, and natural selection pressures that decrease those advantages through reduced survivorship. Predation pressure, as a mode of natural selection, often is invoked as a counter‐selective force to sexual selection, yet few studies have demonstrated empirically that more conspicuous individuals experience higher rates of predation. We quantified predator attacks on models of collared lizards, Crotaphytus collaris, in three well‐studied populations (Oklahoma, USA). These populations differ in coloration and in visual backgrounds against which the lizards are viewed by conspecifics and predators. Attack frequencies varied considerably among study sites but at all sites the models exhibiting the strongest color contrast with local rocks were detected and attacked most often. By comparison, inconspicuous models of females were never attacked at any of the sites. These results suggest a survival cost of conspicuous coloration in collared lizards, and reiterate the importance of considering the visual environment as well as differences among populations when examining the influence of predation on the evolution of animal color patterns.     

Viability selection on prey morphology by a generalist predator

Prey use their locomotory capacity to escape predators, and there should thus be strong viability selection on locomotory morphology of prey. We compared feather morphology of wood pigeons Columba palumbus killed by goshawks Accipiter gentilis with that of survivors to quantify directional and quadratic selection on primary and rectrix feathers. The goshawk is mainly a predator attacking by surprise, leaving wood pigeons with an ability to accelerate fast at a selective advantage. There was directional selection for light primary feathers with a narrow calamus. In addition, there was directional selection for increased area of rectrices. These patterns of natural selection were confirmed in multivariate analyses of selection that showed selection for light primary feathers with a large area and narrow calamus and for a large area of rectrix feathers. These results provide evidence of selection on different aspects of feather morphology directly related to flight performance and thus escape ability from predators.     

Ecological genetics of adaptive color polymorphism in pocket mice: geographic variation in selected and neutral genes

Patterns of geographic variation in phenotype or genotype may provide evidence for natural selection. Here, we compare phenotypic variation in color, allele frequencies of a pigmentation gene (the melanocortin-1 receptor, Mc1r), and patterns of neutral mitochondrial DNA (mtDNA) variation in rock pocket mice (Chaetodipus intermedius) across a habitat gradient in southern Arizona. Pocket mice inhabiting volcanic lava have dark coats with unbanded, uniformly melanic hairs, whereas mice from nearby light-colored granitic rocks have light coats with banded hairs. This color polymorphism is a presumed adaptation to avoid predation. Previous work has demonstrated that two Mc1r alleles, D and d, differ by four amino acids, and are responsible for the color polymorphism: DD and Dd genotypes are melanic whereas dd genotypes are light colored. To determine the frequency of the two Mc1r allelic classes across the dark-colored lava and neighboring light-colored granite, we sequenced the Mc1r gene in 175 individuals from a 35-km transect in the Pinacate lava region. We also sequenced two neutral mtDNA genes, COIII and ND3, in the same individuals. We found a strong correlation between Mc1r allele frequency and habitat color and no correlation between mtDNA markers and habitat color. Using estimates of migration from mtDNA haplotypes between dark- and light-colored sampling sites and Mc1r allele frequencies at each site, we estimated selection coefficients against mismatched Mc1r alleles, assuming a simple model of migration-selection balance. Habitat-dependent selection appears strong but asymmetric: selection is stronger against light mice on dark rock than against melanic mice on light rock. Together these results suggest that natural selection acts to match pocket mouse coat color to substrate color, despite high levels of gene flow between light and melanic populations.     

Population density mediates the interaction between pre‐ and postmating sexual selection

When females mate with more than one male, sexual selection acts both before and after mating. The interaction between pre‐ and postmating episodes of selection is expected to be context dependent, but few studies have investigated how total sexual selection changes under different ecological conditions. We examined how population density mediates the interaction between pre‐ and postmating sexual selection by establishing replicate populations of the horned dung beetle Onthophagus taurus at low, medium, and high densities, and then using microsatellite‐based parentage analyses to measure male fitness. We found that mating success and fertilization success were positively correlated at all three densities, but the strength of the correlation decreased with increasing density. We also found a shift from negative to positive linear selection on testes mass as density increased, and opposing selection on weapons and testes at high densities. These patterns suggest that the importance of postmating processes increases with increasing population density, which reduces the selective advantage of weapons for premating contest competition, and increases the selective advantage of large ejaculates for postmating sperm competition. We expect that density‐dependent selection on testes mass has contributed to the phenotypic variation observed between natural populations of O. taurus that differ in density.     

Antagonistic selection factors induce a continuous population divergence in a polymorphism

Understanding the relative importance of selection and stochastic factors in population divergence of adaptive traits is a classical topic in evolutionary biology. However, it is difficult to separate these factors and detect the effects of selection when two or more contrasting selective factors are simultaneously acting on a single locus. In the damselfly Ischnura senegalensis, females exhibit color dimorphism and morph frequencies change geographically. We here evaluated the role of selection and stochastic factors in population divergence of morph frequencies by comparing the divergences in color locus and neutral loci. Comparisons between population pairwise F_ST for neutral loci and for the color locus did not detect any stochastic factors affecting color locus. Although comparison between population divergence in color and neutral loci using all populations detected only divergent selection, we detected two antagonistic selective factors acting on the color locus, that is, balancing and divergent selection, when considering geographical distance between populations. Our results suggest that a combination of two antagonistic selective factors, rather than stochastic factors, establishes the geographic cline in morph frequency in this system.     

Visual detection and fruit selection by the mantled howler monkey (Alouatta palliata)

Howler monkeys (platyrrhini) have evolved routine trichromatic color vision independently from catarrhines, which presents an opportunity to test hypotheses concerning the adaptive value of distinguishing reddish from greenish hues. A longstanding hypothesis posits that trichromacy aids in the efficient detection of reddish-ripe fruits, which could be an advantage for the detection of the nutritional content of the fruit, such as sugars. In the present study, we assessed fruit visual conspicuity and selection based on color and sucrose content by wild mantled howler monkeys (Alouatta palliata) on Agaltepec Island, Mexico. We used colorimetry to classify dietary fruits as cryptic (greenish) or conspicuous (reddish) against their background leaves. Species-specific color models indicate that trichromatic howler monkeys should be more efficient in discriminating the conspicuous ripe fruits from leaves compared to detecting cryptic ripe fruits from leaves. We found howler monkeys consume more cryptic fruits compared to conspicuous fruits, and that they consume more unripe fruits than ripe fruits. The consumption (acceptance) of fruit was independent of sucrose content, and thus this disaccharide may not play an essential role in mantled howler food selection. Our findings suggest that routine trichromatic color vision may aid in the detection and discrimination of conspicuously colored fruits, but that the final decision whether to accept or reject a fruit probably involves the use of other senses in addition to vision.     

Intensity of male‐male competition predicts morph diversity in a color polymorphic lizard

Sexual selection is one of the main processes involved in the emergence and maintenance of heritable color polymorphisms in a variety of taxa. Here, we test whether the intensity of sexual selection, estimated from population sex ratio, predicts morph diversity in Podarcis muralis, a color polymorphic lizard with discrete white, yellow, orange, white‐orange, and yellow‐orange male and female phenotypes (i.e., morphs). In a sample of 116 Pyrenean populations and 5421 lizards, sex ratios (m/f) vary from 0.29 to 2.5, with the number of morphs for each sex ranging from 2 to 5. Male‐biased sex ratios are associated with increased morph diversity as measured with Shannon's diversity index. The main factor accounting for this relationship is male morph richness (i.e., the number of morphs). In contrast, female morph diversity is not related to sex ratio. These results suggest a relationship between the intensity of male intrasexual competition and male morph diversity. While other selective forces may interact with sexual selection in maintaining the color polymorphisms in P. muralis, this evidence suggests a complex evolutionary scenario possibly involving frequency‐dependent selection of alternative reproductive tactics and/or complex balancing selection.     

CORRELATIONAL SELECTION FOR COLOR PATTERN AND ANTIPREDATOR BEHAVIOR IN THE GARTER SNAKE THAMNOPHIS ORDINOIDES

Correlational selection favors combinations of traits and is a key element of many models of phenotypic and genetic evolution. Multiple regression techniques for measuring selection allow for the direct estimation of correlational selection gradients, yet few studies in natural populations have investigated this process. Color patterns and antipredator behaviors of snakes are thought to function interactively in predator escape and therefore may be subject to correlational selection. To investigate this hypothesis, I studied the survivorship of juvenile garter snakes, Thamnophis ordinoides, as a function of a suite of escape behaviors and color pattern. The only natural selection detected favored opposite combinations of stripedness of the color pattern and the tendency to perform during escape evasive behaviors called reversals. This selection presumably results from optical illusions created by moving patterns and their effects on visually foraging predators. Analysis of the bivariate selection surface shows that pure correlational selection can be thought of as a series of linear selection functions on one trait whose slopes depend on the value of the second trait. Alternatively, viewing the selection surface along its major axes reveals stabilizing and disruptive components of correlational selection. It is further shown that correlational selection alone can promote genetic variance and covariance within a generation. This phenomenon may be partially responsible for the extreme variation in color pattern and the genetic covariance between color pattern and behavior observed in natural populations of T. ordinoides.     

GEOGRAPHIC VARIATION IN FEMALE PREFERENCES FOR MALE TRAITS IN POECILIA RETICULATA

We examined the preferences of female guppies (Poecilia reticulata) from 11 localities in Trinidad with respect to male color-pattern elements, body shape and size, and overall color and brightness contrast. Females are on average more attracted to males from their own population than from alien populations, and populations appear to vary in the criteria used in female choice. Multiple-regression analysis suggests that mate-preference criteria vary among localities in intensity, sign, and the number of traits used. Although preference estimators and color-pattern parameters are unique to each population, only orange, black, and color contrast showed a correlation between degree of male trait and degree of preference for that trait. There is a clear effect of water color and a possible effect of predation intensity. The results are discussed in light of various models of sexual selection and the early stages of speciation.     

Proximate bases of silver color in anhinga (Anhinga anhinga) feathers

Colors of living organisms are produced by selective light absorption from pigments and/or by light scattering from highly ordered nanostructures (i.e., structural color). While the physical bases of metallic colors of arthropods and fish are fairly well‐known, those of birds are not. Here we examine structurally based silver color and its production in feathers of the waterbird species Anhinga. This achromatic color is distinguished from grey by high specular reflectance, from white by low diffuse reflectance, and from both by high gloss. Light and electron microscopy revealed three modifications of feathers likely leading to silver color. First, proximal barbules were highly elongated and contained glossy black color at their base and white color at their pennulum. Second, this glossy black portion contained a single outer layer of keratin weakly bounded by melanosomes. Finally, the white portion contained a disordered amorphous matrix of keratin and air. Optical analyzes suggest that these structures produce, respectively, glossy black color through thin‐film interference and white color through incoherent light scattering. Silver color likely results from the combined reflectance of these adjacent structures. This represents a distinct mechanism for attaining silver colors that may have been partially derived through selection for display, thermoregulation or decreased hydrophobicity. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

SELECTION ON THE COLOR POLYMORPHISM IN HAWAIIAN HAPPY-FACE SPIDERS: EVIDENCE FROM GENETIC STRUCTURE AND TEMPORAL FLUCTUATIONS

Throughout this century genetic polymorphisms for color have been widely used as a research tool to allow insights into key evolutionary processes. Although color variants can often be diverse within populations, frequencies of different morphs may be similar across populations, either as a result of balancing selection or gene flow. Under these circumstances selection can be extremely difficult to demonstrate. Here we test for balancing selection on the naturally occurring color forms of the Hawaiian happy-face spider, Theridion grallator with two approaches. First, allozyme loci are used to generate a null model against which to test selection. Frequencies of alleles involved in the color polymorphism of T. grallator are used to generate another estimate for comparison. The results suggest that statistically similar frequencies of color morphs among populations of T. grallator may be maintained by some form of balancing selection. Second, we make use of an unusual event in which the normally stable frequencies of unpatterned and patterned morphs within a population were found to have shifted toward an excess of unpatterned morphs. We scored offspring of all fertilized, unpatterned (bottom-recessive) females found during this period of skewed morph frequencies and also in a year when morph frequencies were normal to deduce paternal color phenotypes. Mating was found to be random in the normal year, but in the perturbed year females had mated with rare (patterned) males twice as frequently as expected on the basis of the frequency of this morph type in the population. Both of these results are consistent with selection operating on the color polymorphism, and we speculate that apostatic selection, perhaps mediated by bird predators, may provide the mechanism.     

FREQUENCY‐DEPENDENT SOCIAL DOMINANCE IN A COLOR POLYMORPHIC CICHLID FISH

A mechanism commonly suggested to explain the persistence of color polymorphisms in animals is negative frequency‐dependent selection. It could result from a social dominance advantage to rare morphs. We tested for this in males of red and blue color morphs of the Lake Victoria cichlid, Pundamilia. Earlier work has shown that males preferentially attack the males of their own morph, while red males are more likely to win dyadic contests with blue males. In order to study the potential contribution of both factors to the morph co‐existence, we manipulated the proportion of red and blue males in experimental assemblages and studied its effect on social dominance. We then tried to disentangle the effects of the own‐morph attack bias and social dominance of red using simulations. In the experiment, we found that red males were indeed socially dominant to the blue ones, but only when rare. However, blue males were not socially dominant when rare. The simulation results suggest that an own‐morph attack bias reduces the social dominance of red males when they are more abundant. Thus, there is no evidence of symmetric negative frequency‐dependent selection acting on social dominance, suggesting that additional fitness costs to the red morph must explain their co‐existence.     

SPATIOTEMPORAL VARIATION IN LINEAR NATURAL SELECTION ON BODY COLOR IN WILD GUPPIES (POECILIA RETICULATA)

We conducted 10 mark–recapture experiments in natural populations of Trinidadian guppies to test hypotheses concerning the role of viability selection in geographic patterns of male color variation. Previous work has reported that male guppies are more colorful in low‐predation sites than in high‐predation sites. This pattern of phenotypic variation has been theorized to reflect differences in the balance between natural (viability) selection that disfavors bright male color (owing to predation) and sexual selection that favors bright color (owing to female choice). Our results support the prediction that male color is disfavored by viability selection in both predation regimes. However, it does not support the prediction that viability selection against male color is weaker in low‐predation experiments. Instead, some of the most intense bouts of selection against color occurred in low‐predation experiments. Our results illustrate considerable spatiotemporal variation in selection among experiments, but such variation was not generally correlated with local patterns of color diversity. More complex selective interactions, possibly including the indirect effects of predators on variation in mating behavior, as well as other environmental factors, might be required to more fully explain patterns of secondary sexual trait variation in this system.     

Diversifying and Purifying Selection in the Peptide Binding Region of <Emphasis Type="Italic">DRB</Emphasis> in Mammals

The class II genes of the major histocompatibility complex encode proteins which play a crucial role in antigen presentation. They are among the most polymorphic proteins known, and this polymorphism is thought to be the result of natural selection. To understand the selective pressure acting on the protein and to examine possible differences in the evolutionary dynamics among species, we apply maximum likelihood models of codon substitution to analyze the DRB genes of six mammalian species: human, chimpanzee, macaque, tamarin, dog, and cow. The models account for variable selective pressures across codons in the gene and have the power to detect amino acid residues under either positive or negative selection. Our analysis detected positive selection in the DRB genes in each of the six mammals examined. Comparison with structural data reveals that almost all amino acid residues inferred to be under positive selection in humans are in the peptide binding region (PBR) and are in contact with the antigen side chains, although residues outside of but close to the PBR are also detected. Strong purifying selection is also detected in the PBR, at sites which contact the antigen and at sites which may be involved in dimerization or T cell binding. The analysis demonstrates the utility of the random-sites analysis even when structural information is available. The different mammalian species are found to share many positively or negatively selected sites, suggesting that their functional roles have remained very similar in the different species, despite the different habitats and pathogens of the species.     

Impact of the stringency of cell selection on plastid segregation in protoplast fusion-derived Nicotiana regenerates

Summary Vegetative segregation of a mixed plastid population in protoplast fusion-derived cell lines can be directed by a selection favouring the multiplication of one of the parental plastid types. This report defines some of the critical conditions leading to a homogeneous plastid population in cybrid plants generated by protoplast fusion between Nicotiana plumbaginifolia and an albino and streptomycin-resistant N. tabacum plastid mutant. Light (1,500 lx) conferred a strong selective advantage to chloroplasts versus albino plastids, while the lack of this effect in dim light (300 lx) indicated that a sufficient light intensity is essential to the phenomenon. Selection on streptomycin-containing medium in the dark, however, led to the preferential multiplication of resistant plastids. Streptomycin selection of resistant chloroplasts in the light, consequently, results in a plastid selection of doubled stringency. In another experiment a definite, but leaky, selection for chloroplast recombination (selection for greening on streptomycin-containing medium in dim light) was used to reveal various recombination products. Protoplast fusion in fact resulted in cybrid plants showing only simple chimeric segregation of unchanged parental plastids. These results demonstrate the essential requirement for stringent plastid selection, as defined by cell culture conditions, to precede the formation of shoots expected to possess the desired plastid genetic composition.     

Laboratory models,causal explanation and group selection

We develop an account of laboratory models, which have been central to the group selection controversy. We compare arguments for group selection in nature with Darwin's arguments for natural selection to argue that laboratory models provide important grounds for causal claims about selection. Biologists get information about causes and cause-effect relationships in the laboratory because of the special role their own causal agency plays there. They can also get information about patterns of effects and antecedent conditions in nature. But to argue that some cause is actually responsible in nature, they require an inference from knowledge of causes in the laboratory context and of effects in the natural context. This process, cause detection, forms the core of an analogical argument for group selection. We discuss the differing roles of mathematical and laboratory models in constructing selective explanations at the group level and apply our discussion to the units of selection controversy to distinguish between the related problems of cause determination and evaluation of evidence. Because laboratory models are at the intersection of the two problems, their study is crucial for framing a coherent theory of explanation for evolutionary biology.     

SALIVARY ANDROGEN-BINDING PROTEIN (ABP) MEDIATES SEXUAL ISOLATION IN MUS MUSCULUS

We wanted to determine whether the microevolution of the mouse salivary androgen-binding protein (ABP) Alpha subunit gene (Abpa) could mediate sexual selection and thereby have a potential role in maintaining gene pool integrity where radiating mouse subspecies make secondary contact. This hypothesis is based upon previous work in this laboratory, which has shown that each subspecies apparently has its own allele and that these alleles have a 25-fold excess of nonsynonymous/synonymous base substitutions compared to an average protein under purifying selection. We provide direct evidence for ABP-assortative mate selection in a laboratory setting: Mus musculus domesticus and M. m. musculus female mice recognize and discriminate between the territories of male mice that essentially differ solely in their Abpa genotype and, when the males are present, the female prefers to mate with the one of her own ABP type. The observation that females could differentiate between the territories of the two males when those mice were absent suggests that the males marked their territories with ABP. In this study, we also detected ABP on the pelts of male mice and in their environment. It is likely that the animals apply the protein to their pelts by licking and that it is then deposited in their surroundings. We suggest that females of the two subspecies are able to discriminate between males of those subspecies on the basis of this protein molecule. Mouse salivary ABP might present a worthwhile system with which to study a prezygotic isolation mechanism in a mammal.