Marlene Zuk

Sexual selection and speciation

The power of sexual selection to drive changes in mate recognition traits gives it the potential to be a potent force in speciation. Much of the evidence to support this possibility comes from comparative studies that examine differences in the number of species between clades that apparently differ in the intensity of sexual selection. We argue that more detailed studies are needed, examining extinction rates and other sources of variation in species richness. Typically, investigations of extant natural populations have been too indirect to convincingly conclude speciation by sexual selection. Recent empirical work, however, is beginning to take a more direct approach and rule out confounding variables.

Exploitation of sexual signals by predators and parasitoids

Signals used to attract mates are often conspicuous to predators and parasites, and their evolution via sexual selection is expected to be opposed by viability selection. Many secondary sexual traits may represent a compromise between attractiveness and avoidance of detection. Although such signal exploitation appears to be widespread, most examples come from species that use acoustic or olfactory mating signals, and relatively few cases of visual signal exploitation can be substantiated. Because males are usually the signaling sex, they are more at risk from predators or parasitoids that locate prey or hosts by sexual signals; this differential selection on the two sexes can affect the intensity of sexual selection on male ornamental traits. The notable exception to male signaling and female attraction occurs in pheromone-producing insects, particularly lepidopterans, which show an opposite pattern of female odor production. Exploitation of such sex pheromones is relatively rare. We discuss reasons for the reversal in sex roles in these species and its implications for signal exploitation. Changes in signals that appear to be adaptations to avoid predation include the use of different signal modalities, changes in signaling behavior, loss of signals, and alteration of signal characteristics such as pitch. Selection pressure from signal exploiters could lead to the production of a novel signal and thus facilitate speciation. Relatively little work has been done on adaptations on the part of the exploiting species, but such adaptations could indirectly influence the mating system of the predator or parasitoid. Signal exploitation is also expected to be a fruitful source of examples of coevolution. Finally, plants emit attractants analogous to secondary sex characters in animals, and may also be vulnerable to signal exploitation.

Immune defense and host life history.

Recent interest has focused on immune response in an evolutionary context, with particular attention to disease resistance as a life‐history trait, subject to trade‐offs against other traits such as reproductive effort. Immune defense has several characteristics that complicate this approach, however; for example, because of the risk of autoimmunity, optimal immune defense is not necessarily maximum immune defense. Two important types of cost associated with immunity in the context of life history are resource costs, those related to the allocation of essential but limited resources, such as energy or nutrients, and option costs, those paid not in the currency of resources but in functional or structural components of the organism. Resource and option costs are likely to apply to different aspects of resistance. Recent investigations into possible trade‐offs between reproductive effort, particularly sexual displays, and immunity have suggested interesting functional links between the two. Although all organisms balance the costs of immune defense against the requirements of reproduction, this balance works out differently for males than it does for females, creating sex differences in immune response that in turn are related to ecological factors such as the mating system. We conclude that immune response is indeed costly and that future work would do well to include invertebrates, which have sometimes been neglected in studies of the ecology of immune defense.

Sex differences in parasite infections: Patterns and processes

Sex differences in parasite infection rates, intensities, or population patterns are common in a wide range of taxa. These differences are usually attributed to 1 of 2 causes: (1) ecological (sociological in humans); and (2) physiological, usually hormonal in origin. Examples of the first cause include differential exposure to pathogens because of sex-specific behavior or morphology. The second cause may stem from the well-documented association between testosterone and the immune system; sexually mature male vertebrates are often more susceptible to infection and carry higher parasite burdens in the field. Although many researchers favor one explanation over the other, the requisite controlled experiments to rule out confounding variables are often neglected. We suggest that sex differences in disease have evolved just as sex differences in morphology and behavior, and are the result of selection acting differently on males and females. Research has often focused on proximate mechanistic explanations for the sex difference in infection rates, but it is equally important to understand the generality of the patterns in an evolutionary context. Because males potentially gain more than females by taking risks and engaging in competition, sexual selection pressure has shaped male behavior and appearance to maximize competitive ability and attractiveness. Many of the classic male attributes such as antlers on deer are testosterone-dependent, putting males in what appears to be a cruel bind: become vulnerable to disease by developing an attractive secondary sexual ornament, or risk lowered mating success by reducing it. A variety of hypotheses have been put forward to explain why males have not circumvented this dilemma. The mating system of the host species will influence the likelihood of sex differences in parasite infection, because males in monogamous species are subject to weaker sexual selection than males in polygynous species. Whether these evolutionary generalizations apply to invertebrates, which lack testosterone, remains to be seen.

Endocrine-Immune Interactions, Ornaments and Mate Choice in Red Jungle Fowl

Consistently with previous studies, female red jungle fowl (Gallus gallus) preferred to mate with males with longer, redder combs, but paid little attention to plumage characters. Individual variation in comb length was positively correlated with plasma testosterone level. Males with longer combs had fewer circulating lymphocytes, as would be expected if maintenance of secondary sexual characters is costly to the immune system.

Male-male competition, ornamentation and the role of testosterone in sexual selection in red jungle fowl

Abstract Ornamental traits related to success in male-male competition were studied in red jungle fowl, Gallus gallus. In controlled fights between pairs of males, comb size was the only morphological trait that correlated with winning. Among free-ranging, socially integrated groups of 1-year-old males, body size and comb chroma (degree of saturation with pigment), in addition to comb size, were significantly related to dominance. In jungle fowl, the comb is strongly affected by blood testosterone level, which in turn reflects the current physical condition of the individual.

HABITAT SELECTION, ACOUSTIC ADAPTATION, AND THE EVOLUTION OF REPRODUCTIVE ISOLATION

Abstract We examined barriers to gene flow in a hybrid zone of two subspecies of the song sparrow (Melospiza melodia). We focused on how mating signals and mate choice changed along an environmental gradient and gathered data on the morphology, genetics, ecology, and behavior across the zone. Melospiza m. heermanni of the Pacific slope of California and M. m. fallax of the Sonoran Desert, each distinct in plumage, meet across a steep environmental gradient in southeastern California. Although both subspecies occur in riparian habitat, their occupied habitat differs structurally, the former subspecies occurring in areas with denser understory and greater vertical heterogeneity. Song elements varied concomitantly, as predicted by the acoustic adaptation hypothesis, with heermanni having lower‐pitched, more widely spaced elements. Females of both subspecies responded more strongly to homotypic than heterotypic song, and addition of subspecific plumage cues increased response if song was homotypic but not if heterotypic. Females thus assess multiple male traits, weighing song more heavily. Males of both subspecies showed significantly greater agonistic response to homotypic song. Microsatellite variation is correlated significantly with plumage variation across the zone and suggests limited gene flow between the taxa. The association of song and plumage with the environment and in turn with assortative mating suggests a means by which reproductive isolation may evolve or be maintained in hybrid zones.

Disease, Endocrine--Immune Interactions, and Sexual Selection

Parasites and disease have been increasingly recognized as agents of eco- logical and evolutionary importance. Because the endocrine and immune systems are re- lated, it is also likely that hormonally controlled traits, such as secondary sexual characters, may be influenced by responses to disease. Testosterone appears to be associated with a suppressed immune system in many vertebrates, and evidence from captive Red Jungle Fowl suggests that the sexes differ in blood parameters involved in immunity and that comb length is negatively correlated with lymphocyte number in males. Immune system parameters may provide a useful gauge of condition in captive and field-caught animals.

IMMUNE SUPPRESSION AND THE COST OF REPRODUCTION IN THE GROUND CRICKET, ALLONEMOBIUS SOCIUS

Abstract One of the most common life history trade‐offs in animals is the reduction in survivorship with increasing reproductive effort. Despite the prevalence of this pattern, its underlying physiological mechanisms are not well understood. Here we test the hypothesis that immune suppression mediates this phenotypic trade‐off by manipulating reproductive effort and measuring immune function and mortality rates in the striped ground cricket, Allonemobius socius. Because A. socius males provide females with a hemolymph‐based nuptial gift during copulation, and many structural components of immunity reside in the hemolymph, we also predicted that sexual selection may differentially affect how disease resistance evolves in males and females. We found that an increased mating effort resulted in a reduced immune ability, coupled with an increased rate in age‐specific mortality for both sexes. Thus, immune suppression appears to be a link between reproductive effort and cost in this system. In addition, males and females appeared to differentially invest in several aspects of immunity prior to mating, with males exhibiting a higher concentration of circulating hemocytes and a superior bacterial defense capability. This pattern may be the result of previously established positive selection on gift size due to its affect on female fecundity. In short, female choice for larger gifts may lead to a sexually dimorphic immune ability.

Same-sex sexual behavior and evolution

Same-sex sexual behavior has been extensively documented in non-human animals. Here we review the contexts in which it has been studied, focusing on case studies that have tested both adaptive and non-adaptive explanations for the persistence of same-sex sexual behavior. Researchers have begun to make headway unraveling possible evolutionary origins of these behaviors and reasons for their maintenance in populations, and we advocate expanding these approaches to examine their role as agents of evolutionary change. Future research employing theoretical, comparative and experimental approaches could provide a greater understanding not only of how selection might have driven the evolution of same-sex sexual behaviors but also ways in which such behaviors act as selective forces that shape social, morphological and behavioral evolution.