Joel W. McGlothlin

Publications

• Hormones and the evolution of behavior and other complex phenotypes

  E. D. Ketterson, J. W. Atwell, J. W. McGlothlin

  01/2012;
• 5.43

  Impact points

  Phenotypic assortment mediates the effect of social selection in a wild beetle population.

  Vincent A Formica, Joel W McGlothlin, Corlett W Wood, Malcolm E Augat, Rebecca E Butterfield, Mollie E Barnard, Edmund D Brodie

  Evolution; international journal of organic evolution. 10/2011; 65(10):2771-81.

  Social interactions often have major fitness consequences, but little is known about how specific interacting phenotypes affect the strength of natural selection. Social influences on the evolutionary process can be assessed using a multilevel selection approach that partitions the effects of social... [more] Social interactions often have major fitness consequences, but little is known about how specific interacting phenotypes affect the strength of natural selection. Social influences on the evolutionary process can be assessed using a multilevel selection approach that partitions the effects of social partner phenotypes on fitness (referred to as social or group selection) from those of the traits of a focal individual (nonsocial or individual selection). To quantify the contribution of social selection to total selection affecting a trait, the patterns of phenotypic association among interactants must also be considered. We estimated selection gradients on male body size in a wild population of forked fungus beetles (Bolitotherus cornutus). We detected positive nonsocial selection and negative social selection on body size operating through differences in copulation success, indicating that large males with small social partners had highest fitness. In addition, we found that, in low-density demes, the phenotypes of focal individuals were negatively correlated with those of their social partners. This pattern reversed the negative effect of group selection on body size and led to stronger positive selection for body size. Our results demonstrate multilevel selection in nature and stress the importance of considering social selection whenever conspecific interactions occur nonrandomly.
• 4.11

  Impact points

  Promiscuous mating produces offspring with higher lifetime fitness.

  Nicole M Gerlach, Joel W McGlothlin, Patricia G Parker, Ellen D Ketterson

  Proceedings. Biological sciences / The Royal Society. 08/2011; 279(1730):860-6.

  In many species, each female pairs with a single male for the purpose of rearing offspring, but may also engage in extra-pair copulations. Despite the prevalence of such promiscuity, whether and how multiple mating benefits females remains an open question. Multiple mating is typically thought to be... [more] In many species, each female pairs with a single male for the purpose of rearing offspring, but may also engage in extra-pair copulations. Despite the prevalence of such promiscuity, whether and how multiple mating benefits females remains an open question. Multiple mating is typically thought to be favoured primarily through indirect benefits (i.e. heritable effects on the fitness of offspring). This prediction has been repeatedly tested in a variety of species, but the evidence has been equivocal, perhaps because such studies have focused on pre-reproductive survival rather than lifetime fitness of offspring. Here, we show that in a songbird, the dark-eyed junco (Junco hyemalis), both male and female offspring produced by extra-pair fertilizations have higher lifetime reproductive success than do offspring sired within the social pair. Furthermore, adult male offspring sired via extra-pair matings are more likely to sire extra-pair offspring (EPO) themselves, suggesting that fitness benefits to males accrue primarily through enhanced mating success. By contrast, female EPO benefited primarily through enhanced fecundity. Our results provide strong support for the hypothesis that the evolution of extra-pair mating by females is favoured by indirect benefits and shows that such benefits accrue much later in the offspring's life than previously documented.
• 5.43

  Impact points

  Interacting phenotypes and the evolutionary process. III. Social evolution.

  Joel W McGlothlin, Allen J Moore, Jason B Wolf, Edmund D Brodie

  Evolution; international journal of organic evolution. 09/2010; 64(9):2558-74.

  Interactions among conspecifics influence social evolution through two distinct but intimately related paths. First, they provide the opportunity for indirect genetic effects (IGEs), where genes expressed in one individual influence the expression of traits in others. Second, interactions can genera... [more] Interactions among conspecifics influence social evolution through two distinct but intimately related paths. First, they provide the opportunity for indirect genetic effects (IGEs), where genes expressed in one individual influence the expression of traits in others. Second, interactions can generate social selection when traits expressed in one individual influence the fitness of others. Here, we present a quantitative genetic model of multivariate trait evolution that integrates the effects of both IGEs and social selection, which have previously been modeled independently. We show that social selection affects evolutionary change whenever the breeding value of one individual covaries with the phenotype of its social partners. This covariance can be created by both relatedness and IGEs, which are shown to have parallel roles in determining evolutionary response. We show that social selection is central to the estimation of inclusive fitness and derive a version of Hamilton's rule showing the symmetrical effects of relatedness and IGEs on the evolution of altruism. We illustrate the utility of our approach using altruism, greenbeards, aggression, and weapons as examples. Our model provides a general predictive equation for the evolution of social phenotypes that encompasses specific cases such as kin selection and reciprocity. The parameters can be measured empirically, and we emphasize the importance of considering both IGEs and social selection, in addition to relatedness, when testing hypotheses about social evolution.
• 4.80

  Impact points

  Natural selection on testosterone production in a wild songbird population.

  Joel W McGlothlin, Danielle J Whittaker, Sara E Schrock, Nicole M Gerlach, Jodie M Jawor, Eric A Snajdr, Ellen D Ketterson

  The American naturalist. 06/2010; 175(6):687-701.

  Because of their role in mediating life-history trade-offs, hormones are expected to be strongly associated with components of fitness; however, few studies have examined how natural selection acts on hormonal variation in the wild. In a songbird, the dark-eyed junco (Junco hyemalis), field experime... [more] Because of their role in mediating life-history trade-offs, hormones are expected to be strongly associated with components of fitness; however, few studies have examined how natural selection acts on hormonal variation in the wild. In a songbird, the dark-eyed junco (Junco hyemalis), field experiments have shown that exogenous testosterone alters individuals' resolution of the survival-reproduction trade-off, enhancing reproduction at the expense of survival. Here we used standardized injections of gonadotropin-releasing hormone (GnRH) to assay variation in the testosterone production of males. Using measurements of annual survival and reproduction, we found evidence of strong natural selection acting on GnRH-induced increases in testosterone. Opposite to what would be predicted from the survival-reproduction trade-off, patterns of selection via survival and reproduction were remarkably similar. Males with GnRH-induced testosterone production levels that were slightly above the population mean were more likely to survive and also produced more offspring, leading to strong stabilizing selection. Partitioning reproduction into separate components revealed positive directional selection via within-pair siring success and stabilizing selection via extrapair mating success. Our data represent the most complete demonstration of natural selection on hormones via multiple fitness components, and they complement previous experiments to illuminate testosterone's role in the evolution of life-history trade-offs.
• 5.43

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  COMBINING SELECTIVE EPISODES TO ESTIMATE LIFETIME NONLINEAR SELECTION.

  Joel W McGlothlin

  Evolution; international journal of organic evolution. 12/2009;

  Studies measuring natural selection acting via different components of fitness may provide insight into such central questions in evolutionary biology as the evolution of life histories and sexual dimorphism. It is often desirable to combine estimates of selection at different episodes to understand... [more] Studies measuring natural selection acting via different components of fitness may provide insight into such central questions in evolutionary biology as the evolution of life histories and sexual dimorphism. It is often desirable to combine estimates of selection at different episodes to understand how they interact to produce total lifetime selection. When selective episodes are sequential, total directional selection may be calculated by summing directional selection across episodes. However, it is unclear whether lifetime nonlinear (e.g. stabilizing, disruptive, or correlational) selection may be similarly calculated using estimates of quadratic selection from sequential episodes. Here, I show that lifetime quadratic selection depends not only upon the sum total of quadratic selection across episodes but also upon the pattern of directional selection across episodes. In certain cases, the effects of directional selection across episodes may cancel one another, leading to no net directional selection but strong stabilizing selection. This result suggests that true stabilizing selection may be more common than previously thought, especially when the entire life cycle is considered. The equations derived here are easily applicable to empirical data, as is illustrated both with a simulated dataset and with a reanalysis of a study of quadratic selection in dark-eyed juncos.
• 1.98

  Impact points

  Phenotypic integration and independence: Hormones, performance, and response to environmental change.

  Ellen D Ketterson, Jonathan W Atwell, Joel W McGlothlin

  Integrative and comparative biology. 10/2009; 49(4):365-79.

  Hormones coordinate the co-expression of behavioral, physiological, and morphological traits, giving rise to correlations among traits and organisms whose parts work well together. This article considers the implications of these hormonal correlations with respect to the evolution of hormone-mediate... [more] Hormones coordinate the co-expression of behavioral, physiological, and morphological traits, giving rise to correlations among traits and organisms whose parts work well together. This article considers the implications of these hormonal correlations with respect to the evolution of hormone-mediated traits. Such traits can evolve owing to changes in hormone secretion, hormonal affinity for carrier proteins, rates of degradation and conversion, and interaction with target tissues to name a few. Critically, however, we know very little about whether these changes occur independently or in tandem, and thus whether hormones promote the evolution of tight phenotypic integration or readily allow the parts of the phenotype to evolve independently. For example, when selection favors a change in expression of hormonally mediated characters, is that alteration likely to come about through changes in hormone secretion (signal strength), changes in response to a fixed level of secretion (sensitivity of target tissues), or both? At one extreme, if the phenotype is tightly integrated and only the signal responds via selection's action on one or more hormonally mediated traits, adaptive modification may be constrained by past selection for phenotypic integration. Alternatively, response to selection may be facilitated if multivariate selection favors new combinations that can be easily achieved by a change in signal strength. On the other hand, if individual target tissues readily "unplug" from a hormone signal in response to selection, then the phenotype may be seen as a loose confederation that responds on a trait-by-trait basis, easily allowing adaptive modification, although perhaps more slowly than if signal variation were the primary mode of evolutionary response. Studies reviewed here and questions for future research address the relative importance of integration and independence by comparing sexes, individuals, and populations. Most attention is devoted to the hormone testosterone (T) and a songbird species, the dark-eyed junco (Junco hyemalis).
• 6.03

  Impact points

  Contribution of direct and maternal genetic effects to life-history evolution.

  Laura F Galloway, Julie R Etterson, Joel W McGlothlin

  The New phytologist. 08/2009;

  * Maternal effects are ubiquitous in nature. In plants, most work has focused on the effects of maternal environments on offspring trait expression. Less is known about the prevalence of genetic maternal effects and how they influence adaptive evolution. Here, we used multivariate genetic models to ... [more] * Maternal effects are ubiquitous in nature. In plants, most work has focused on the effects of maternal environments on offspring trait expression. Less is known about the prevalence of genetic maternal effects and how they influence adaptive evolution. Here, we used multivariate genetic models to estimate the contributions of maternal and direct genetic (co)variance, the cross-generation direct-maternal covariance, and M, the matrix of maternal effect coefficients, for life-history traits in Campanulastrum americanum, a monocarpic herb. * Following a three-generation breeding design, we grew paternal half-sib families with full-sib relatives of each parent and measured juvenile and adult traits. * Seed size was influenced exclusively by maternal environmental effects, whereas maternal genetic effects influenced traits throughout the life cycle, including strong direct and maternal additive genetic correlations within and between generations for phenological and size traits. Examination of M suggested that both juvenile and adult traits in maternal plants influenced the expression of offspring traits. * This study reveals substantial potential for genetic maternal effects to contribute to adaptive evolution including cross-generation direct-maternal correlations that may slow selection response, maternal effects on phenology that reinforce genetic correlations, and within- and between-generation genetic correlations that may influence life-history polymorphism.
• 5.43

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  HOW TO MEASURE INDIRECT GENETIC EFFECTS: THE CONGRUENCE OF TRAIT-BASED AND VARIANCE-PARTITIONING APPROACHES.

  Joel W McGlothlin, Edmund D Brodie

  Evolution; international journal of organic evolution. 03/2009;

  Indirect genetic effects (IGEs), which occur when phenotypic expression in one individual is influenced by genes in another conspecific individual, may have a drastic effect on evolutionary response to selection. General evolutionary models of IGEs have been developed using two distinct theoretical ... [more] Indirect genetic effects (IGEs), which occur when phenotypic expression in one individual is influenced by genes in another conspecific individual, may have a drastic effect on evolutionary response to selection. General evolutionary models of IGEs have been developed using two distinct theoretical frameworks derived from maternal effects theory. The first framework is trait-based and focuses on how phenotypes are influenced by specific traits in a social partner, with the strength of interactions defined by the matrix Psi. The second framework partitions total genetic variance into components representing direct effects, indirect effects, and the covariance between them, without identifying specific social traits responsible for IGEs. The latter framework has been employed more commonly by empiricists because the methods for estimating variance components are relatively straightforward. Here, we show how these two theoretical frameworks are related to each other and derive equations that can be used to translate between them. This translation leads to a generalized method that can be used to estimate Psi via standard quantitative genetic breeding designs or pedigrees from natural populations. This method can be used in a very general set of circumstances and is widely applicable to all IGEs, including maternal effects and other interactions among relatives.
• 5.12

  Impact points

  Hormone-mediated suites as adaptations and evolutionary constraints.

  Joel W McGlothlin, Ellen D Ketterson

  Philosophical transactions of the Royal Society of London. Series B, Biological sciences. 06/2008; 363(1497):1611-20.

  Hormones mediate the expression of suites of correlated traits and hence may act both to facilitate and constrain adaptive evolution. Selection on one trait within a hormone-mediated suite may, for example, lead to a change in the strength of the hormone signal, causing either beneficial or detrimen... [more] Hormones mediate the expression of suites of correlated traits and hence may act both to facilitate and constrain adaptive evolution. Selection on one trait within a hormone-mediated suite may, for example, lead to a change in the strength of the hormone signal, causing either beneficial or detrimental changes in correlated traits. Theory and empirical methods for studying correlated trait evolution have been developed by the field of evolutionary quantitative genetics, and here we suggest that their application to the study of hormone-mediated suites may prove fruitful. We present hypotheses for how selection shapes the evolution of hormone-mediated suites and argue that correlational selection, which arises when traits interact in their effects on fitness, may act to alter or conserve the composition of hormone-mediated suites. Next, we advocate using quantitative genetic methods to assess natural covariation among hormone-mediated traits and to measure the strength of natural selection acting on them. Finally, we present illustrative examples from our own work on the evolution of testosterone-mediated suites in male and female dark-eyed juncos. We conclude that future work on hormone-mediated suites, if motivated by quantitative genetic theory, may provide important insights into their dual roles as adaptations and evolutionary constraints.
• 3.82

  Impact points

  Hormones and honest signals: males with larger ornaments elevate testosterone more when challenged.

  J W McGlothlin, J M Jawor, T J Greives, J M Casto, J L Phillips, E D Ketterson

  Journal of evolutionary biology. 02/2008; 21(1):39-48.

  When male investment in mating varies with quality, reliable sexual signals may evolve. In many songbirds, testosterone mediates mating investment, suggesting that signals should be linked to testosterone production. However, because testosterone may change rapidly during behaviour such as territori... [more] When male investment in mating varies with quality, reliable sexual signals may evolve. In many songbirds, testosterone mediates mating investment, suggesting that signals should be linked to testosterone production. However, because testosterone may change rapidly during behaviour such as territorial aggression and courtship, efforts to establish such a relationship have proved challenging. In a population of dark-eyed juncos, we measured individual variation in the production of short-term testosterone increases by injecting gonadotropin-releasing hormone (GnRH). We found a positive correlation between the magnitude of these increases and the size of a plumage ornament ('tail white') previously shown to be important for female choice and male-male competition. We then measured naturally elevated testosterone levels produced during male-male competition and found that they covaried with those induced by GnRH. We suggest that the association between tail white and testosterone increases may allow conspecifics to assess potential mates and competitors reliably using tail white.
• 4.80

  Impact points

  Natural variation in a testosterone-mediated trade-off between mating effort and parental effort.

  Joel W McGlothlin, Jodie M Jawor, Ellen D Ketterson

  The American naturalist. 01/2008; 170(6):864-75.

  Male birds frequently face a trade-off between acquiring mates and caring for offspring. Hormone manipulation studies indicate that testosterone often mediates this trade-off, increasing mating effort while decreasing parental effort. Little is known, however, about individual covariation between te... [more] Male birds frequently face a trade-off between acquiring mates and caring for offspring. Hormone manipulation studies indicate that testosterone often mediates this trade-off, increasing mating effort while decreasing parental effort. Little is known, however, about individual covariation between testosterone and relevant behavior on which selection might act. Using wild, male dark-eyed juncos (Junco hyemalis), we measured individual variation in testosterone levels before and after standardized injections of gonadotropin-releasing hormone (GnRH). The GnRH challenges have been shown to produce short-term testosterone increases that are similar to those produced naturally in response to social stimuli, repeatable in magnitude, and greater in males with more attractive ornaments. We correlated these testosterone increases with behavioral measures of mating and parental effort (aggressive response to a simulated territorial intrusion and nestling feeding, respectively). Males that showed higher postchallenge testosterone displayed more territorial behavior, and males that produced higher testosterone increases above initial levels displayed reduced parental behavior. Initial testosterone levels were positively but nonsignificantly correlated with aggression but did not predict parental behavior. These relationships suggest that natural variation in testosterone, specifically the production of short-term increases, may underlie individual variation in the mating effort/parental effort trade-off. We discuss the implications of these results for the evolution of hormonally mediated trade-offs.
• 3.82

  Impact points

  A cautionary tale of two matrices: the duality of multivariate abstraction.

  E D Brodie, J W McGlothlin

  Journal of evolutionary biology. 02/2007; 20(1):9-14; discussion 39-44.

• Testosterone response to GnRH in a female songbird varies with stage of reproduction: implications for adult behaviour and maternal effects.

  J. M. Jawor, J. W. McGlothlin, J. M. Casto, T. J. Greives, E. A. Snajdr, G. E. Bentley, E. D. Ketterson.

  Functional Ecology. 01/2007; 21:767-775.
• 2.75

  Impact points

  Diet quality affects feather growth rate and an attractive white plumage pattern in dark-eyed juncos (Junco hyemalis)

  J. W. McGlothlin, D. L. Duffy, J. L. Henry-Freeman, E. D. Ketterson.

  Behavioral Ecology and Sociobiology. 01/2007; 61:1391-1399.

• Testosterone and immune function inversely co-vary in a wild population of breeding Dark-eyed Juncos (Junco hyemalis)

  T. J. Greives, J. W. McGlothlin, J. M. Jawor, G. E. Demas, E. D. Ketterson

  Functional Ecology. 01/2007; 20:812-818.
• 2.73

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  Seasonal and individual variation in response to GnRH challenge in male dark-eyed juncos (Junco hyemalis).

  Jodie M Jawor, Joel W McGlothlin, Joseph M Casto, Timothy J Greives, Eric A Snajdr, George E Bentley, Ellen D Ketterson

  General and comparative endocrinology. 12/2006; 149(2):182-9.

  Concentrations of gonadal steroids such as testosterone (T) often vary widely in natural populations, but the causes and particularly the consistency of this variation is relatively unexplored. In breeding males of a wild population of the dark-eyed junco (Junco hyemalis), we investigated seasonal a... [more] Concentrations of gonadal steroids such as testosterone (T) often vary widely in natural populations, but the causes and particularly the consistency of this variation is relatively unexplored. In breeding males of a wild population of the dark-eyed junco (Junco hyemalis), we investigated seasonal and individual variation in circulating T during two breeding seasons by measuring the responsiveness of the HPG axis to a standardized injection of gonadotropin-releasing hormone (GnRH). Individuals were bled prior to and 30min after injection. Pre- and post-challenge levels of T were measured using EIA. Many subjects were sampled repeatedly across multiple breeding stages. Plasma T concentrations nearly doubled in response to GnRH during early spring, but showed significantly smaller increases in later breeding stages. When controlling for seasonal variation in response to challenge, we also found repeatable differences among individuals, indicating individual consistency in the release of T in response to a standardized stimulus. These seasonal and individual differences may arise from comparable variation in responsiveness of the pituitary or a decline in gonadal sensitivity to downstream gonadotropins. In contrast, pre-challenge T showed almost no seasonal changes and did not differ consistently among individuals. To our knowledge, this is the first demonstration of individual repeatability of short-term hormonal changes in a wild population. Such repeatability suggests that hormonal plasticity might evolve in response to changing selection pressures.
• 5.43

  Impact points

  Correlational selection leads to genetic integration of body size and an attractive plumage trait in dark-eyed juncos.

  Joel W McGlothlin, Patricia G Parker, Val Nolan, Ellen D Ketterson

  Evolution; international journal of organic evolution. 04/2005; 59(3):658-71.

  When a trait's effect on fitness depends on its interaction with other traits, the resultant selection is correlational and may lead to the integration of functionally related traits. In relation to sexual selection, when an ornamental trait interacts with phenotypic quality to determine mating ... [more] When a trait's effect on fitness depends on its interaction with other traits, the resultant selection is correlational and may lead to the integration of functionally related traits. In relation to sexual selection, when an ornamental trait interacts with phenotypic quality to determine mating success, correlational sexual selection should generate genetic correlations between the ornament and quality, leading to the evolution of honest signals. Despite its potential importance in the evolution of signal honesty, correlational sexual selection has rarely been measured in natural populations. In the dark-eyed junco (Junco hyemalis), males with experimentally elevated values of a plumage trait (whiteness in the tail or "tail white") are more attractive to females and dominant in aggressive encounters over resources. We used restricted maximum-likelihood analysis of a long-term dataset to measure the heritability of tail white and two components of body size (wing length and tail length), as well as genetic correlations between pairs of these traits. We then used multiple regression to assess directional, quadratic, and correlational selection as they acted on tail white and body size via four components of lifetime fitness (juvenile and adult survival, mating success, and fecundity). We found a positive genetic correlation between tail white and body size (as measured by wing length), which indicates past correlational selection. Correlational selection, which was largely due to sexual selection on males, was also found to be currently acting on the same pair of traits. Larger males with whiter tails sired young with more females, most likely due to a combination of female choice, which favors males with whiter tails, and male-male competition, which favors both tail white and larger body size. To our knowledge, this is the first study to show both genetic correlations between sexually selected traits and currently acting correlational sexual selection, and we suggest that correlational sexual selection frequently may be an important mechanism for maintaining the honesty of sexual signals.
• 4.11

  Impact points

  Elevated testosterone reduces choosiness in female dark-eyed juncos (Junco hyemalis): evidence for a hormonal constraint on sexual selection?

  Joel W McGlothlin, Diane L H Neudorf, Joseph M Casto, Val Nolan, Ellen D Ketterson

  Proceedings. Biological sciences / The Royal Society. 08/2004; 271(1546):1377-84.

  Because testosterone (T) often mediates the expression of attractive displays and ornaments, in the absence of constraints sexual selection should lead to an evolutionary increase in male T levels. One candidate constraint would be a genetic correlation between the sexes that leads to a correlated r... [more] Because testosterone (T) often mediates the expression of attractive displays and ornaments, in the absence of constraints sexual selection should lead to an evolutionary increase in male T levels. One candidate constraint would be a genetic correlation between the sexes that leads to a correlated response in females. If increased T in females were to have deleterious effects on mate choice, the effect of sexual selection on male T would be weakened. Using female dark-eyed juncos (Junco hyemalis), we tested whether experimentally enhancing female T would lead to a decrease in discrimination between two classes of males, one treated with T (T-males) and one control (C-males). The two female treatments (T-implanted and C-females) spent equal amounts of time with both classes of males, but T-treated females failed to show a preference for either male treatment, whereas C-females showed a significant preference, albeit in an unexpected direction (for C-males). T-females were less discriminating than C-females, irrespective of the direction of their preference. To our knowledge, this is the first study to show that circulating hormones can alter female choosiness without reducing sexual motivation. Our results suggest that hormonal correlations between the sexes have the potential to constrain sexual selection on males.
• 0.86

  Impact points

  Revisit schedule does not affect results of point counts

  M. A. Brooks, B. C. Harrigan, K. M. Johnson, D. E. Lowe, J. P. Lowery, J. W. McGlothlin, M. M. Sasso, S. A. Smith, D. A. Cristol

  Journal of Field Ornithology. 01/2001; 72:404-411.