W. Edwin Harris

Reproductive investment when mate quality varies: differential allocation versus reproductive compensation

Reproductive investment decisions form an integral part of life-history biology. Selection frequently favours plasticity in investment that can generate maternal effects on offspring development. For example, if females differentially allocate resources based on mate attractiveness or quality, this can create a non-genetic link between mate attractiveness and offspring fitness with potential consequences for ecological and evolutionary dynamics. It is therefore important to understand under what conditions differential investment into offspring in relation to male quality is expected to occur and the direction of the effect. Two opposite predictions, increased investment into offspring produced with high-quality mates (differential allocation (DA)) and increased investment with low-quality males (reproductive compensation (RC)) have been suggested but no formal theoretical treatment justifying the assumptions underlying these two hypotheses has been conducted to date. Here, we used a state-based approach to investigate the circumstances under which the variation in mate quality results in differential female investment into offspring and how this interacts with female energetic resource levels. We found that a pattern of increased investment when mating with high-quality mates (i.e. DA) was the most common optimal investment strategy for females in our model. By contrast, increased investment when mating with low-quality mates (i.e. RC) was predicted only when the relative impact of parental investment on offspring quality was low. Finally, we found that the specific pattern of investment in relation to male quality depends on female energetic state, the likelihood for future mating opportunities and the expected future distribution of mate quality. Thus, the females age and body condition should be important factors mediating DA and RC, which may help to explain the equivocal results of empirical studies.

CONSTRAINTS ON EVOLUTION AND POSTCOPULATORY SEXUAL SELECTION: TRADE-OFFS AMONG EJACULATE CHARACTERISTICS

Abstract . Ejaculates function as an integrated unit to ensure male fertility and paternity, can have a complex structure, and can experience multiple episodes of selection. Current studies on the evolution of ejaculates typically focus on phenotypic variation in sperm number, size, or related traits such as testes size as adaptations to postcopulatory male‐male competition. However, the evolution of the integrated nature of ejaculate structure and function depends on genetic variation in and covariation between the component parts. Here we report a quantitative genetic study of the components of the ejaculate of the cockroach Nauphoeta cinerea, including those we know to experience postcopulatory sexual selection, in the context of functional integration of ejaculate characters. We use the patterns of genetic variation and covariation to infer how the integration of the functions of the ejaculate constrain and shape its evolution. Ejaculate components were highly variable, showed significant additive genetic variance, and moderate to high evolvability. The level of genetic variation in these characters, despite strong directional or truncating selection, may reflect the integration of multiple episodes of selection that occur in N. cinerea. There were few significant phenotypic correlations, but all the genetic correlations among ejaculate characters were significantly different from zero. The patterns of genetic variation and covariation suggest that there are important trade‐offs among individual traits of the ejaculate and that evolution of ejaculate characteristics will not proceed unconstrained. Fully describing the genetic relationships among traits that perform as an integrated unit helps us understand how functional relationships constrain or facilitate the evolution of the complex structure that is the ejaculate.

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. Hum Mutat 0, 1–7, 2008.

Female mate preference and sexual conflict: females prefer males that have had fewer consorts.

Different aspects of male quality as a mate can vary independently. When this is the case, females may need to use multiple cues to accurately assess overall mate quality. We examined the pattern of mating preference in the cockroach Nauphoeta cinerea. Sexual conflict occurs in this species because male manipulation of female mating receptivity can result in reduced female fitness. We predicted that since females cannot remate within a single reproductive bout because of male manipulation, females should assess male mating history to avoid mating with males with low fertility caused by sperm exhaustion. In a mate‐preference experiment, we found that females discriminated against males who had mated multiple times. Females also discriminated against males who had consorted with several females but had been prevented from mating with those females. Thus, females appeared to be able to detect cues on males that were derived from previous mates and to use this information to avoid mating with sperm‐exhausted males. We suggest that females may commonly use multiple cues to assess different aspects of mate quality, especially when male quality changes over time. This is an under‐studied phenomenon that could help explain individual variation in female mating preferences.

Influence of Double-Gloving on Manual Dexterity and Tactile Sensation of Surgeons

BACKGROUND Double-gloving in the performance of surgical procedures has been demonstrated to reduce the frequency of blood contact with the hands of members of the surgical team. Concerns persist that double-gloving can compromise the dexterity and tactile sensitivity of the surgeon. STUDY DESIGN Fifty-three surgeons and surgeons-in-training volunteered at the Clinical Congress of the American College of Surgeons and were studied using the Purdue Pegboard test and a standard 2-point discrimination test to compare no gloves, a single pair of gloves, and double-gloving on manual dexterity and tactile sensitivity. Categorical and continuous variables were identified, general linear prediction models were computed, and the influence of glove status was analyzed as an independent variable. Monte Carlo simulation was employed to validate conclusions. RESULTS Gender, specialty, and handedness did not affect prediction models. Glove status did not affect dexterity performance scores (p = 0.57) after accounting for the influence of age on score variation (p < 0.001). Comparing ulnar and radial surfaces of the index finger for 2-point discrimination, no difference was detected between trials (p < 0.66), nor was an interaction effect detected with glove status (p = 0.40). Monte Carlo simulations validated the apparent absence of differences. CONCLUSIONS Double-gloving does not have a substantial impact on manual dexterity or tactile sensitivity when compared with no gloves or single-gloving in this study.

Sperm competition within a dominance hierarchy: investment in social status vs. investment in ejaculates

There is increasing recognition that male–male competition can take many forms, but as yet the form is not predictable a priori. Many recent studies have focused attention on how males in disadvantaged mating roles compensate through sperm competition. However, mating systems in which subordinate males are reproductively suppressed, particularly through the stress of social interactions, may limit the ability of males to respond by increasing investment in sperm quality. We examined the interaction between social status and ejaculate tactics in Nauphoeta cinerea, a cockroach that has a mating system with well‐characterized dominance hierarchies. Both social experience with other males and social status influenced aspects of ejaculates. The stress of social interactions reduced the size of the ejaculate and number of sperm inseminated. In ejaculates formed prior to social experience, however, males that go on to become dominant inseminated more sperm than males that go on to become subordinate, suggesting innate differences among males. Our results show that though selection for increased success in sperm competition for subordinate males in a hierarchy can occur, both the traits and the way in which the balance between pre‐ and post‐copulatory strategies is negotiated will depend on specific details of the mating system. These details will include how the physiological effects of social interactions may limit selection through male–male competition.

Is a decline in offspring quality a necessary consequence of maternal age

Recent studies in two species of Drosophila have demonstrated a negative effect of parental age on offspring fitness, including a reduced hatch rate of eggs and larval-to-adult viability. This has led to a call to consider the decline of offspring quality as a function of parental age in theoretical considerations of the evolution of ageing. We have tested whether a decline in egg and larval quality of older mothers is a general feature of senescence by examining it in the cockroach Nauphoeta cinerea. We also tested whether maternal age affected the reproductive potential of daughters. Although maternal age at first reproduction profoundly affected maternal fitness, there was no difference in hatch rate or larval viability between the offspring of young and old mothers. Likewise, the reproductive potential of the daughters of young and old mothers was the same. Thus, while maternal age effects may be important aspects of ageing in some systems, the generality and overall importance for theories of ageing remain unclear.

The capture of heritable variation for genetic quality through social competition

In theory, females of many species choose mates based on traits that are indicators of male genetic quality. A fundamental question in evolutionary biology is why genetic variation for such indicator traits persists despite strong persistent selection imposed by female preference, which is known as the lek paradox. One potential solution to the lek paradox suggests that the traits that are targets of mate choice should evolve condition-dependent expression and that condition should have a large genetic variance. Condition is expected to exhibit high genetic variance because it is affected by a large number of physiological processes and hence, condition-dependent traits should ‘capture’ variation contributed by a large number of loci. We suggest that a potentially important cause of variation in condition is competition for limited resources. Here, we discuss a pair of models to analyze the evolutionary genetics of traits affected by success in social competition for resources. We show that competition can contribute to genetic variation of ‘competition-dependent’ traits that have fundamentally different evolutionary properties than other sources of variation. Competition dependence can make traits honest indicators of genetic quality by revealing the relative competitive ability of males, can provide a component of heritable variation that does not contribute to trait evolution, and can help maintain heritable variation under directional selection. Here we provide a general introduction to the concept of competition dependence and briefly introduce two models to demonstrate the potential evolutionary consequences of competition-dependent trait expression.

The Maintenance of Heritable Variation Through Social Competition

Abstract The paradoxical persistence of heritable variation for fitness-related traits is an evolutionary conundrum that remains a preeminent problem in evolutionary biology. Here we describe a simple mechanism in which social competition results in the evolutionary maintenance of heritable variation for fitness related traits. We demonstrate this mechanism using a genetic model with two primary assumptions: the expression of a trait depends upon success in social competition for limited resources; and competitive success of a genotype depends on the genotypes that it competes against. We find that such social competition generates heritable (additive) genetic variation for “competition-dependent” traits. This heritable variation is not eroded by continuous directional selection because, rather than leading to fixation of favored alleles, selection leads instead to allele frequency cycling due to the concerted coevolution of the social environment with the effects of alleles. Our results provide a mechanism for the maintenance of heritable variation in natural populations and suggest an area for research into the importance of competition in the genetic architecture of fitness related traits.

Sex-Biased Inbreeding Effects on Reproductive Success and Home Range Size of the Critically Endangered Black Rhinoceros

A central premise of conservation biology is that small populations suffer reduced viability through loss of genetic diversity and inbreeding. However, there is little evidence that variation in inbreeding impacts individual reproductive success within remnant populations of threatened taxa, largely due to problems associated with obtaining comprehensive pedigree information to estimate inbreeding. In the critically endangered black rhinoceros, a species that experienced severe demographic reductions, we used model selection to identify factors associated with variation in reproductive success (number of offspring). Factors examined as predictors of reproductive success were age, home range size, number of nearby mates, reserve location, and multilocus heterozygosity (a proxy for inbreeding). Multilocus heterozygosity predicted male reproductive success (p< 0.001, explained deviance >58%) and correlated with male home range size (p < 0.01, r(2) > 44%). Such effects were not apparent in females, where reproductive success was determined by age (p < 0.01, explained deviance 34%) as females raise calves alone and choose between, rather than compete for, mates. This first report of a 3-way association between an individual males heterozygosity, reproductive output, and territory size in a large vertebrate is consistent with an asymmetry in the level of intrasexual competition and highlights the relevance of sex-biased inbreeding for the management of many conservation-priority species. Our results contrast with the idea that wild populations of threatened taxa may possess some inherent difference from most nonthreatened populations that necessitates the use of detailed pedigrees to study inbreeding effects. Despite substantial variance in male reproductive success, the increased fitness of more heterozygous males limits the loss of heterozygosity. Understanding how individual differences in genetic diversity mediate the outcome of intrasexual competition will be essential for effective management, particularly in enclosed populations, where individuals have restricted choice about home range location and where the reproductive impact of translocated animals will depend upon the background distribution in individual heterozygosity.