REACTION NORMS OF MORPHOLOGICAL AND LIFE-HISTORY TRAITS TO LIGHT AVAILABILITY IN IMPATIENS CAPENSIS

For plants, light availability is an important environmental factor that varies both within and between populations. Although the existence of sun and shade “ecotypes” is controversial, it is often assumed that trade-offs may exist between performance in sun and in shade. This study therefore investigated variation in reaction norms to light availability within and between two neighboring natural populations of the annual Impatiens capensis, one in full sun and the other in a forest understory. Seedlings were collected randomly from both populations and grown to maturity in a greenhouse under two light conditions: full light and 18% of full light. Selfed full-sib seed families were collected from plants from both populations grown in both parental light environments. To characterize family reaction norms, seedlings from each family were divided into the same two light treatments and individuals were scored for a variety of morphological and life-history traits. The maternal light environment had little impact on progeny reaction norms. However, the two study populations differed both qualitatively and quantitatively in plastic response to light availability (indicated by significant population x environment interactions in mixed-model ANCOVA). Much of this difference was attributable to population differences in light sensitivity of axillary meristem allocation patterns, which produced concurrent differences in reaction norms for a suite of developmentally linked traits. Within each population, different sets of traits displayed significant variation in plasticity (indicated by significant family x environment interactions). Thus, the genetic potential for evolutionary response to selection in heterogeneous light environments may differ dramatically between neighboring plant populations. Between-environment genetic correlations were largely positive in the woods population and positive or nonsignificant in the sun population; there was no evidence for performance trade-offs across environments or sun or shade “specialist” genotypes within either population. There was little evidence that population differences represented adaptive differentiation for sun or shade; rather, the results suggested the hypothesis of differential selection on patterns of meristem allocation caused by population differences in timing of mortality and intensity of competition.     

EVOLUTION OF STATIC ALLOMETRIES: ADAPTIVE CHANGE IN ALLOMETRIC SLOPES OF EYE SPAN IN STALK‐EYED FLIES

Julian Huxley showed that within‐species (static) allometric (power‐law) relations can arise from proportional growth regulation with the exponent in the power law equaling the factor of proportionality. Allometric exponents may therefore be hard to change and act as constraints on the independent evolution of traits. In apparent contradiction to this, many empirical studies have concluded that static allometries are evolvable. Many of these studies have been based, however, on a broad definition of allometry that includes any monotonic shape change with size, and do not falsify the hypothesis of constrained narrow‐sense allometry. Here, we present the first phylogenetic comparative study of narrow‐sense allometric exponents based on a reanalysis of data on eye span and body size in stalk‐eyed flies (Diopsidae). Consistent with a role in sexual selection, we found strong evidence that male slopes were tracking “optima” based on sexual dimorphism and relative male trait size. This tracking was slow, however, with estimated times of 2–3 million years for adaptation to exceed ancestral influence on the trait. Our results are therefore consistent with adaptive evolution on million‐year time scales, but cannot rule out that static allometry may act as a constraint on eye‐span adaptation at shorter time scales.     

QUANTITATIVE GENETICS AND THE EVOLUTION OF REACTION NORMS

We extend methods of quantitative genetics to studies of the evolution of reaction norms defined over continuous environments. Our models consider both spatial variation (hard and soft selection) and temporal variation (within a generation and between generations). These different forms of environmental variation can produce different evolutionary trajectories even when they favor the same optimal reaction norm. When genetic constraints limit the types of evolutionary changes available to a reaction norm, different forms of environmental variation can also produce different evolutionary equilibria. The methods and models presented here provide a framework in which empiricists may determine whether a reaction norm is optimal and, if it is not, to evaluate hypotheses for why it is not.     

GENETIC DRIFT IN ANTAGONISTIC GENES LEADS TO DIVERGENCE IN SEX‐SPECIFIC FITNESS BETWEEN EXPERIMENTAL POPULATIONS OF DROSOPHILA MELANOGASTER

Males and females differ in their reproductive roles and as a consequence are often under diverging selection pressures on shared phenotypic traits. Theory predicts that divergent selection can favor the invasion of sexually antagonistic alleles, which increase the fitness of one sex at the detriment of the other. Sexual antagonism can be subsequently resolved through the evolution of sex‐specific gene expression, allowing the sexes to diverge phenotypically. Although sexual dimorphism is very common, recent evidence also shows that antagonistic genetic variation continues to segregate in populations of many organisms. Here we present empirical data on the interaction between sexual antagonism and genetic drift in populations that have independently evolved under standardized conditions. We demonstrate that small experimental populations of Drosophila melanogaster have diverged in male and female fitness, with some populations showing high male, but low female fitness while other populations show the reverse pattern. The between‐population patterns are consistent with the differentiation in reproductive fitness being driven by genetic drift in sexually antagonistic alleles. We discuss the implications of our results with respect to the maintenance of antagonistic variation in subdivided populations and consider the wider implications of drift in fitness‐related genes.     

PHENOTYPIC PLASTICITY AND REACTION NORMS IN TEMPERATE AND TROPICAL POPULATIONS OF DROSOPHILA MELANOGASTER: OVARIAN SIZE AND DEVELOPMENTAL TEMPERATURE

The plasticity of ovariole number relative to developmental temperature was studied in three populations of Drosophila melanogaster at both ends of the cline: a temperate French population and two equatorial Congolese. Ovary size was much greater in the French flies, in agreement with an already known latitudinal cline. Among isofemale lines, significant differences in genetic variability were observed between populations with a maximum variability at intermediate temperatures. Parameters of phenotypic variability (CV and FA) were not statistically different among lines or populations, but a significant increase at low temperature was demonstrated for both. The shapes of the response curves (i.e., the norm of reaction) were analyzed by adjusting the data to a quadratic equation. The parameters of the equation were highly variable among lines. On the other hand, the temperature for maximum value of ovarioles (TMV) was much less variable and exhibited only a slightly significant difference between temperate and tropical flies (22.2°C vs. 22.7°C). During its geographic extension toward colder places, D. melanogaster underwent a large, presumably adaptative, increase in ovariole number but very little change in the norm of reaction of that trait.     

MACROEVOLUTIONARY PATTERNS OF MORPHOLOGICAL DIVERSIFICATION AMONG PARASITIC FLATWORMS (PLATYHELMINTHES: CERCOMERIA)

Patterns of parasite morphological diversification were investigated using a morphological data base for the parasitic platyhelminths comprising 1,459 characters analyzed using phylogenetic systematic methods. Only 10.8% of the 1,882 character transformations are losses, casting doubt on views that parasites are secondarily simplified and exhibit degenerate evolution. Chi-squared analysis indicates that character loss in the Digenea and Monogenea occurs in proportion to total change and is disproportionately lower within the Eucestoda. In the Digenea fewer female characters and more male characters have been lost than expected by the total number of characters in that group, and more male and more nonreproductive characters have been lost in proportion to their distribution across groups. In the Monogenea fewer nonreproductive and more larval characters have been lost than expected within the group, and female character loss is high relative to other groups. In the Eucestoda fewer female and more larval characters have been lost than expected within the group, whereas loss of male and nonreproductive character is low, and loss of larval characters is high, compared to the other groups. Patterns of character loss result partially from characters that show repeated (homoplasious) loss in different groups. High consistency index and low homoplasy slope ratio values indicate that the parasitic platyhelminths show unusually low levels of homoplasy, casting doubt on views that parasite morphology is unusually adaptively plastic. Homoplasy within the monogeneans occurs in proportion to overall character change, is slightly higher than expected in the digeneans, and is much lower than expected within the eucestodes. Homoplasy occurs less often than expected in larval characters, and more often than expected in nonreproductive characters in the Digenea. Monogeneans show more homoplasy than expected for larval characters both within and among groups. Eucestodes show fewer homoplasious male and nonreproductive, and more homoplasious larval, characters than expected within the group, and higher homoplasy in larval characters and lower homoplasy in female and nonreproductive characters among groups.     

SEX LINKAGE,SEX‐SPECIFIC SELECTION,AND THE ROLE OF RECOMBINATION IN THE EVOLUTION OF SEXUALLY DIMORPHIC GENE EXPRESSION

Sex‐biased genes—genes that are differentially expressed within males and females—are nonrandomly distributed across animal genomes, with sex chromosomes and autosomes often carrying markedly different concentrations of male‐ and female‐biased genes. These linkage patterns are often gene‐ and lineage‐dependent, differing between functional genetic categories and between species. Although sex‐specific selection is often hypothesized to shape the evolution of sex‐linked and autosomal gene content, population genetics theory has yet to account for many of the gene‐ and lineage‐specific idiosyncrasies emerging from the empirical literature. With the goal of improving the connection between evolutionary theory and a rapidly growing body of genome‐wide empirical studies, we extend previous population genetics theory of sex‐specific selection by developing and analyzing a biologically informed model that incorporates sex linkage, pleiotropy, recombination, and epistasis, factors that are likely to vary between genes and between species. Our results demonstrate that sex‐specific selection and sex‐specific recombination rates can generate, and are compatible with, the gene‐ and species‐specific linkage patterns reported in the genomics literature. The theory suggests that sexual selection may strongly influence the architectures of animal genomes, as well as the chromosomal distribution of fixed substitutions underlying sexually dimorphic traits.     

PHENOTYPIC PLASTICITY IN POLYGONUM PERSICARIA. I. DIVERSITY AND UNIFORMITY IN GENOTYPIC NORMS OF REACTION TO LIGHT

Several aspects of genotype-environment interaction may act to modulate natural selection in populations that encounter variable environments. In this study the norms of reaction (phenotypic responses) of 20 cloned genotypes from two natural populations of the annual plant Polygonum persicaria were determined over a broad range of controlled light environments (8%-100% full sun). These data reveal both the extent of functionally adaptive phenotypic plasticity expressed by individual genotypes, and the patterns of diversity among genotypes for characters relevant to fitness, in response to an environmental factor that is both highly variable within populations and critical to growth and reproduction.     

SEX‐SPECIFIC EVOLUTIONARY POTENTIAL OF PRE‐ AND POSTCOPULATORY REPRODUCTIVE INTERACTIONS IN THE FIELD CRICKET,TELEOGRYLLUS COMMODUS

Mate choice often depends on the properties of both sexes, such as the preference and responsiveness of the female and the sexual display traits of the male. Quantitative genetic studies, however, traditionally explore the outcome of an interaction between males and females based solely on the genotype of one sex, treating the other sex as a source of environmental variance. Here, we use a half‐sib breeding design in the field cricket, Teleogryllus commodus, to estimate the additive genetic contribution of both partners to three steps of the mate choice process: the time taken to mate; the duration of spermatophore attachment; and the intensity of mate guarding. Rather than each sex contributing equally to the interactions, we found that genetic variation for latency to mate and spermatophore attachment was sex‐specific, and in the case of mate‐guarding intensity, largely absent. For a given interaction, genetic variation in one sex also appears to be largely independent of the other, and is also uncorrelated with the other traits. We discuss how pre‐ and postcopulatory interactions have the potential to evolve as an interacting phenotype, but that any coevolution between these traits, due to sexual selection or sexual conflict, may be limited.     

PHENOTYPIC PLASTICITY IN POLYGONUM PERSICARIA. II. NORMS OF REACTION TO SOIL MOISTURE AND THE MAINTENANCE OF GENETIC DIVERSITY

Adaptive phenotypic plasticity is the predicted evolutionary response to fine-grained fluctuation in major environmental factors, such as soil moisture in plant habitats. This study examines genotypes from two natural populations of Polygonum persicaria, one from a relatively homogeneous, moderately moist site, and one from a site in which severe drought and root flooding occur within single growth seasons. Norms of reaction (phenotypic response curves) were determined for a random sample of eight and ten cloned genotypes, respectively, from each of the populations over a controlled moisture gradient ranging from drought to flooding.     

COMPARATIVE FUNCTIONAL ANALYSES OF ULTRABITHORAX REVEAL MULTIPLE STEPS AND PATHS TO DIVERSIFICATION OF LEGS IN THE ADAPTIVE RADIATION OF SEMI‐AQUATIC INSECTS

Invasion of new ecological habitats is often associated with lineage diversification, yet the genetic changes underlying invasions and radiations are poorly understood. Over 200 million years ago, the semi‐aquatic insects invaded water surface from a common terrestrial ancestor and diversified to exploit a wide array of niches. Here, we uncover the changes in regulation and function of the gene Ultrabithorax associated with both the invasion of water surface and the subsequent diversification of the group. In the common ancestor of the semi‐aquatic insects, a novel deployment of Ubx protein in the mid‐legs increased their length, thereby enhancing their role in water surface walking. In derived lineages that specialize in rowing on the open water, additional changes in the timing of Ubx expression further elongated the mid‐legs thereby facilitating their function as oars. In addition, Ubx protein function was selectively reversed to shorten specific rear‐leg segments, thereby enabling their function as rudders. These changes in Ubx have generated distinct niche‐specialized morphologies that account for the remarkable diversification of the semi‐aquatic insects. Therefore, changes in the regulation and function of a key developmental gene may facilitate both the morphological change necessary to transition to novel habitats and fuel subsequent morphological diversification.     

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.     

SEXUAL SELECTION AND THE EVOLUTION OF COMPLEX COLOR PATTERNS IN DRAGON LIZARDS

Many species have elaborate and complex coloration and patterning, which often differ between the sexes. Sexual selection may increase the size or intensity of color patches (elaboration) in one sex or drive the evolution of novel signal elements (innovation). The latter potentially increases color pattern complexity. Color pattern complexity may also be influenced by ecological factors related to predation and environment; however, very few studies have investigated the effects of both sexual and natural selection on color pattern complexity across species. We used a phylogenetic comparative approach to examine these effects in 85 species and subspecies of Australian dragon lizards (family Agamidae). We quantified color pattern complexity by adapting the Shannon–Wiener diversity index. There were clear sex differences in color pattern complexity, which were positively correlated with both sexual dichromatism and sexual size dimorphism, consistent with the idea that sexual selection plays a significant role in the evolution of color pattern complexity. By contrast, we found little evidence of a link between environmental factors and color pattern complexity on body regions exposed to predators. Our results suggest that sexual selection rather than natural selection has led to increased color pattern complexity in males.     

GENETIC,MORPHOLOGICAL, AND ACOUSTIC EVIDENCE REVEALS LACK OF DIVERSIFICATION IN THE COLONIZATION PROCESS IN AN ISLAND BIRD

Songbirds with recently (i.e., early Holocene) founded populations are suitable models for studying incipient differentiation in oceanic islands. On such systems each colonization event represents a different evolutionary episode that can be studied by addressing sets of diverging phenotypic and genetic traits. We investigate the process of early differentiation in the spectacled warbler (Sylvia conspicillata) in 14 populations separated by sea barriers from three Atlantic archipelagos and from continental regions spanning from tropical to temperate latitudes. Our approach involved the study of sexual acoustic signals, morphology, and genetic data. Mitochondrial DNA did not provide clear population structure. However, microsatellites analyses consistently identified two genetic groups, albeit without correspondence to subspecies classification and little correspondence to geography. Coalescent analyses showed significant evidence for gene flow between the two genetic groups. Discriminant analyses could not correctly assign morphological or acoustic traits to source populations. Therefore, although theory predicting that in isolated populations genetic, morphological, or acoustic traits can lead to radiation, we have strikingly failed to document differentiation on these attributes in a resident passerine throughout three oceanic archipelagos.     

RAPID EVOLUTION OF ASYMMETRIC REPRODUCTIVE INCOMPATIBILITIES IN STALK‐EYED FLIES

The steps by which isolated populations acquire reproductive incompatibilities remain poorly understood. One potentially important process is postcopulatory sexual selection because it can generate divergence between populations in traits that influence fertilization success after copulation. Here we present a comprehensive analysis of this form of reproductive isolation by conducting reciprocal crosses between variably diverged populations of stalk‐eyed flies (Teleopsis dalmanni). First, we measure seven types of reproductive incompatibility between copulation and fertilization. We then compare fertilization success to hatching success to quantify hybrid inviability. Finally, we determine if sperm competition acts to reinforce or counteract any incompatibilities. We find evidence for multiple incompatibilities in most crosses, including failure to store sperm after mating, failure of sperm to reach the site of fertilization, failure of sperm to fertilize eggs, and failure of embryos to develop. Local sperm have precedence over foreign sperm, but this effect is due mainly to differences in sperm transfer and reduced hatching success. Crosses between recently diverged populations are asymmetrical with regard to the degree and type of incompatibility. Because sexual conflict in these flies is low, postcopulatory sexual selection, rather than antagonistic coevolution, likely causes incompatibilities due to mismatches between male and female reproductive traits.     

ORIGINS,EVOLUTION, AND DIVERSIFICATION OF CLEPTOPARASITIC LINEAGES IN LONG‐TONGUED BEES

The evolution of parasitic behavior may catalyze the exploitation of new ecological niches yet also binds the fate of a parasite to that of its host. It is thus not clear whether evolutionary transitions from free‐living organism to parasite lead to increased or decreased rates of diversification. We explore the evolution of brood parasitism in long‐tongued bees and find decreased rates of diversification in eight of 10 brood parasitic clades. We propose a pathway for the evolution of brood parasitic strategy and find that a strategy in which a closed host nest cell is parasitized and the host offspring is killed by the adult parasite represents an obligate first step in the appearance of a brood parasitic lineage; this ultimately evolves into a strategy in which an open host cell is parasitized and the host offspring is killed by a specialized larval instar. The transition to parasitizing open nest cells expanded the range of potential hosts for brood parasitic bees and played a fundamental role in the patterns of diversification seen in brood parasitic clades. We address the prevalence of brood parasitic lineages in certain families of bees and examine the evolution of brood parasitism in other groups of organisms.     

EVOLUTION IN A CONSTANT ENVIRONMENT: THERMAL FLUCTUATIONS AND THERMAL SENSITIVITY OF LABORATORY AND FIELD POPULATIONS OF MANDUCA SEXTA

Adaptation to temporal variation in environmental conditions is widespread. Whether evolution in a constant environment alters adaptation to temporal variation is relatively unexplored. We examine how constant and diurnally fluctuating temperature conditions affect life-history traits in two populations of the tobacco hornworm, Manduca sexta : a field population that routinely experiences fluctuating temperatures; and a laboratory population (derived from this field population in the 1960s) maintained at a constant temperature for more than 250 generations. Our experiments demonstrate that diurnal fluctuations significantly alter body size and development time in both populations, and confirm that these populations differ in their responses to a mean temperature. However, we found no evidence for population divergence in responses to diurnal temperature fluctuations. We suggest that mean and extreme temperatures may act as more potent selective forces on thermal reaction norms than temperature variation per se.     

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.     

ELEVATED RATES OF MORPHOLOGICAL AND FUNCTIONAL DIVERSIFICATION IN REEF‐DWELLING HAEMULID FISHES

The relationship between habitat complexity and species richness is well established but comparatively little is known about the evolution of morphological diversity in complex habitats. Reefs are structurally complex, highly productive shallow‐water marine ecosystems found in tropical (coral reefs) and temperate zones (rocky reefs) that harbor exceptional levels of biodiversity. We investigated whether reef habitats promote the evolution of morphological diversity in the feeding and locomotion systems of grunts (Haemulidae), a group of predominantly nocturnal fishes that live on both temperate and tropical reefs. Using phylogenetic comparative methods and statistical analyses that take into account uncertainty in phylogeny and the evolutionary history of reef living, we demonstrate that rates of morphological evolution are faster in reef‐dwelling haemulids. The magnitude of this effect depends on the type of trait; on average, traits involved in the functional systems for prey capture and processing evolve twice as fast on reefs as locomotor traits. This result, along with the observation that haemulids do not exploit unique feeding niches on reefs, suggests that fine‐scale trophic niche partitioning and character displacement may be driving higher rates of morphological evolution. Whatever the cause, there is growing evidence that reef habitats stimulate morphological and functional diversification in teleost fishes.