Tristan A.F. Long - PhD

T.A.F. Long, A. Pischedda and W.R. Rice. 2010. Remating in Drosophila melanogaster: Are indirect benefits condition-dependent? Evolution [In Press: link coming soon]

Abstract: By measuring the direct and indirect fitness costs and benefits of sexual interactions, the feasibility of alternate explanations for polyandry can be experimentally assessed. This approach becomes more complicated when the relative magnitude of the costs and benefits associated with multiple mating (i.e. remating with different males) vary with female condition. Here, using the model organism Drosophila melanogaster, we test whether the indirect benefits that a non-virgin female gains by remating (trading-up) are influenced by her condition (body size). We found that remating by small-bodied, low-fecundity females resulted in the production of daughters of higher fecundity, while the opposite pattern was observed for large bodied females. In contrast, remating had no measurable effect on the relative reproductive success of sons from dams of either body size. These results are consistent with a hypothesis based on sexually antagonistic genetic variation. The implications of these results to our understanding of the evolution and consequences of polyandry are discussed.

T.A.F. Long, A. Pischedda, R.V. Nichols and W.R. Rice. 2010. The timing of mating influences reproductive success in Drosophila melanogaster: implications for sexual conflict. Journal of Evolutionary Biology [online early LINK]

Abstract: Despite its potential importance, the role of the timing of mating(s) as a source of variation in female lifetime reproductive success has been largely overlooked. Here, using a laboratory-adapted population of the model species Drosophila melanogaster, we explore how temporal variation in the patterns of single and multiple matings influences female fecundity. We find that the boost to fecundity known to occur after a virgin female's initial mating also extends to subsequent matings as nonvirgins, but only for a short duration. This fecundity boost at least partially offsets the direct costs of multiple matings to females in this population of D. melanogaster. The implications of these results for our understanding of the evolution and maintenance of polyandry in this species are discussed in the context of sexual conflict.

T.A.F. Long, A. Pischedda, A.D. Stewart and W.R. Rice. 2009. A Cost of Sexual Attractiveness to High-Fitness Females. PLoS Biology 7(12): e1000254. [LINK]

Abstract: Adaptive mate choice by females is an important component of sexual selection in many species. The evolutionary consequences of male mate preferences, however, have received relatively little study, especially in the context of sexual conflict, where males often harm their mates. Here, we describe a new and counterintuitive cost of sexual selection in species with both male mate preference and sexual conflict via antagonistic male persistence: male mate choice for high-fecundity females leads to a diminished rate of adaptive evolution by reducing the advantage to females of expressing beneficial genetic variation. We then use a Drosophila melanogaster model system to experimentally test the key prediction of this theoretical cost: that antagonistic male persistence is directed toward, and harms, intrinsically higher-fitness females more than it does intrinsically lower-fitness females. This asymmetry in male persistence causes the tails of the population's fitness distribution to regress towards the mean, thereby reducing the efficacy of natural selection. We conclude that adaptive male mate choice can lead to an important, yet unappreciated, cost of sex and sexual selection.

A companion primer paper by Dr. Russel Bonduriansky (University of New South Wales) can be found here.

The UCSB Press Release can be found here.

Follow these links to read how this story was reported by: Science Now, the Australian Broadcasting Company, the National Geographic News, The Santa Barbara Independent and The Santa Barbara News-Press and The Telegraph.

T.A.F. Long, P.M. Miller, A.D. Stewart and W.R. Rice. 2009. Estimating the heritability of adult female fitness in a locally adapted Drosophila melanogaster population. Journal of Evolutionary Biology. 22: 637-643.

Abstract: The heritability of genome-wide fitness that is expected in finite populations is poorly understood, both theoretically and empirically, despit its relevance to many fundamental concepts in evolutionary biology. In this study, we used two independent methds of estimating the heritability of lifetime female fecundity (the predominant female fitness component in this population) in a large, outbred population of Drosophila melanogaster that had adapted to the laboratory environment for over 400 generations. Despite strong directional selection on adult female fecundity, we uncovered high heritability for this trait that cannot be explained by antogonitic pleiotropy with juvenile fitness. The evolutionary significance of this high heritability of lifetime fecundity is discussed.

T.A.F. Long, A.D. Stewart and P.M. Miller. 2009. Potential confounds to an assay of cross-generational fitness benefits of mating and male seminal fluid. Biology Letters. 5: 26-27.

In this review paper, we discusss our concerns regarding the results and conclusions of the paper "Cross-generational fitness benefits of mating and male seminal fluid. 2008. Biology Letters. 4: 6-8." which can be found here.

Priest et al.'s response to our review can be found here.

T.A.F. Long and W.R. Rice. 2007. Adult locomotory activity mediates intralocus sexual conflict in a laboratory-adapted population of Drosophila melanogaster. Proceeding of the Royal Society of London, Series B. 274: 3105-3112.

Abstract: The strongest form of intralocus sexual conflict occurs when two conditions are met: (i) there is a positive intersexual genetic correlation for a trait and (ii) the selection gradients on the trait in the two sexes are in opposite directions. Intralocus sexual conflict can constrain the adaptive evolution of both sexes and thereby contribute to a species' 'gender load'. Previous studies of adult lifetime fitness of the same sets of genes expressed in both males and females have established that there is substantial intralocus conflict in the LHM laboratory-adapted population of Drosophila melanogaster. Here, we investigated whether a highly dimorphic trait-adult locomotory activity-contributed substantially to the established intralocus sexual conflict. To measure the selection gradient on activity level, both this trait and adult lifetime fitness were measured under the same environmental conditions to which the flies were adapted. We found significant phenotypic variation in both sexes for adult locomotory activity, and that the selection gradients on this variation were large and in opposite directions in the two sexes. Using hemiclonal analysis to screen 99% of the entire genome, we found abundant genetic variation for adult locomotory activity and showed that this variation occurs on both the X and autosomes. We also established that there is a strong positive intersexual genetic correlation for locomotory activity. These assays revealed that, despite the strong, extant sexual dimorphism for the trait, locomotory activity continues to contribute strongly to intralocus sexual conflict in this population.

Note: For electronic supplementary material please click here:

T.A.F. Long, R. Montgomerie and A. Chippindale. 2006. Quantifying the gender load: can population crosses reveal interlocus sexual conflict? Philosophical Transactions of the Royal Society of London, Series B. 361: 363-374.

Abstract: If interlocus sexual conflict drives the evolution of reproductive characters, then females are expected to be best-defended against (or least sensitive to) the specific manipulative traits of males in their breeding population. However, depending upon the nature of the coevolving signal-receiver system, crosses between different populations of the same species can theoretically lead to a negative or positive impact of foreign males on female fitness. Using a long-term, laboratory-evolved phylogeny of replicate Drosophila melanogaster populations, we show that intersexual coevolution is rapid and leads to interactions that strongly and directly influence female net fitness, mating, and sperm use patterns. The tendency (19/30 crosses) for foreign males to negatively influence female fitness may be interpreted as evidence for either sexually antagonistic coevolution or the disruption of mutualistically coevolved interactions. Rather, we suggest that instances in which female fitness was improved by mating with foreign males may better reveal the extent of sexual conflict, signaling release from the gender load established by antagonistic coevolution. Variation in both female mating rate and male post-copulatory fitness in response to matings between females and local versus foreign males also showed that populations had diverged in a manner consistent with interlocus sexual conflict.

This paper was presented at the discussion meeting "Sexual conflic: a new paradigm?", hosted by the Royal Society of London. More information on this event can be found here:

T.A.F. Long and R. Montgomerie. 2005. Ejaculate investment in a promiscuous rodent, Peromyscus maniculatus: effects of population density and social role. Evolutionary Ecology Research. 8: 345-356.

Abstract: Questions: How does average male investment into ejaculates vary with changing population density (and thus with the risk of sperm competition) in a promiscuous species? Do individual male investment strategies vary with population density?
Data Studied: Total testes mass, somatic mass and annual population density for wild-caught male deer mice, Peromyscus maniculatus, collected by snap-trapping over a 23-year period in Algonquin Provincial Park, ON, Canada.
Search Methods: We analyzed the relation between mean testes mass and mouse population densities across years. To investigate individual investment patterns, we compared the relation between total testes mass and somatic mass among males for years differing in population density.
Conclusions: Average investment into testes was positively correlated with annual population density. An individual's investment into testes depended on both the abundance of rival males and on relative body size, a trait associated with social rank.

T.A.F. Long and A. Pischedda 2005. Do female Drosophila melanogaster adaptively bias offspring sex ratios in relation to the age of their mate? Proceedings of the Royal Society of London, Series B. 272: 1781-1787.

Abstract. Modification of offspring sex ratios in response to parental quality is predicted when the long-term fitness returns of sons and daughters differ. One factor that may influence a mother's sex allocation decision is the quality (or attractiveness) of her mate. We investigated whether the sex ratios of offspring produced by female Drosophila melanogaster are biased with respect to the age of the males to which they are mated, and whether there is an adaptive basis for this phenomenon. We found that females mated to old males (13d post-eclosion) initially produced a greater proportion of daughters than did females mated to young males (1d post-eclosion). This pattern does not appear to be due to a systematic difference in the numbers or mortality of the X- and Y-bearing sperm originating from old and young fathers, as the overall sex ratios of all offspring produced from a single copulation did not differ between broods fathered by the two types of males. The sons of older males fared worse in competitive mating assays than did the sons of younger males, while daughters of old and young males were of comparable fitness. These results suggest that there is an adaptive basis for the observed sex ratio modification.

Science Now's coverage of this paper can be read here:

T.A.F. Long. 2005. The influence of mating system on the intensity of parent-offspring conflict in primates. Journal of Evolutionary Biology. 18: 509-515.

Abstract: An evolutionary conflict of interest exists between parents and their offspring over the partitioning of parental investment (PI) among siblings. When the direct fitness benefits to offspring of increased PI, outweigh the inclusive fitness costs from lost future sibling fitness, selection should favour the evolution of offspring selfishness over altruism. In theory, this conflict is heightened when females are not strictly monogamous, as current offspring should be less altruistic towards future half-siblings than they would be towards full-siblings. Using data collected on foetal growth rate (representing prenatal PI) in primates, I test the prediction from theory that the resolution of the parent-offspring conflict will be closer to the offspring's evolutionary optima in polyandrous species than in more monandrous species. Using phylogenetic comparative analysis, and controlling for allometry, I show that offspring are able to obtain more PI when the probability of future full-siblings decreases, and that this is most pronounced in taxa where there is the opportunity for direct foetal access to the maternal bloodstream. These results support the hypothesis that the resolution of prenatal PI conflict is influenced by both a species' mating system and by its placental structure.

C. Lewis and T.A.F. Long 2005. Courtship and reproduction in Carybdea sivickisi (Cnidaria: Cubozoa) Marine Biology.147: 477-483.

Abstract: Courtship and fertilization events in cubozoans have received little attention from biologists, and much of what we know about these processes is based on conjecture or scant anecdotal evidence. I set out to describe these processes in the cubozoan Carybdea sivickisi by observing mature medusae in vitro. Mature adults engage in courtship during which spermatophores are transferred from the male to the female, who then inserts the gametes into her manubrium. Females accepted multiple spermatophores from multiple males, and only produced one embryo strand. This study also provides evidence that the presence of conspicuous velar spots on the females bell margin is a signal of sexual maturity, and that sexual maturity was not reached in either sex until individuals had a bell diameter of at least 5 mm.

Non Refereed Publication

Seminal Advances in Sexual Selection. Report on 2003 Biology of Spermatozoa Conference. Inintially published on (now defunct) Biomednet.com. Now located here.



*T.A.F. Long, A. Pischedda and W.R. Rice. 2010. Remating in Drosophila melanogaster: Are indirect benefits condition-dependent? Evolution [In Press: link coming soon]* Abstract: By measuring the direct and indirect fitness costs and benefits of sexual interactions, the feasibility of alternate explanations for polyandry can be experimentally assessed. This approach becomes more complicated when the relative magnitude of the costs and benefits associated with multiple mating (i.e. remating with different males) vary with female condition. Here, using the model organism Drosophila melanogaster, we test whether the indirect benefits that a non-virgin female gains by remating (trading-up) are influenced by her condition (body size). We found that remating by small-bodied, low-fecundity females resulted in the production of daughters of higher fecundity, while the opposite pattern was observed for large bodied females. In contrast, remating had no measurable effect on the relative reproductive success of sons from dams of either body size. These results are consistent with a hypothesis based on sexually antagonistic genetic variation. The implications of these results to our understanding of the evolution and consequences of polyandry are discussed. T.A.F. Long, A. Pischedda, R.V. Nichols and W.R. Rice. 2010. The timing of mating influences reproductive success in Drosophila melanogaster: implications for sexual conflict. Journal of Evolutionary Biology [online early LINK] Abstract: Despite its potential importance, the role of the timing of mating(s) as a source of variation in female lifetime reproductive success has been largely overlooked. Here, using a laboratory-adapted population of the model species Drosophila melanogaster, we explore how temporal variation in the patterns of single and multiple matings influences female fecundity. We find that the boost to fecundity known to occur after a virgin female's initial mating also extends to subsequent matings as nonvirgins, but only for a short duration. This fecundity boost at least partially offsets the direct costs of multiple matings to females in this population of D. melanogaster. The implications of these results for our understanding of the evolution and maintenance of polyandry in this species are discussed in the context of sexual conflict. T.A.F. Long, A. Pischedda, A.D. Stewart and W.R. Rice. 2009. A Cost of Sexual Attractiveness to High-Fitness Females. PLoS Biology 7(12): e1000254. [LINK] Abstract: Adaptive mate choice by females is an important component of sexual selection in many species. The evolutionary consequences of male mate preferences, however, have received relatively little study, especially in the context of sexual conflict, where males often harm their mates. Here, we describe a new and counterintuitive cost of sexual selection in species with both male mate preference and sexual conflict via antagonistic male persistence: male mate choice for high-fecundity females leads to a diminished rate of adaptive evolution by reducing the advantage to females of expressing beneficial genetic variation. We then use a Drosophila melanogaster model system to experimentally test the key prediction of this theoretical cost: that antagonistic male persistence is directed toward, and harms, intrinsically higher-fitness females more than it does intrinsically lower-fitness females. This asymmetry in male persistence causes the tails of the population's fitness distribution to regress towards the mean, thereby reducing the efficacy of natural selection. We conclude that adaptive male mate choice can lead to an important, yet unappreciated, cost of sex and sexual selection. A companion primer paper by Dr. Russel Bonduriansky (University of New South Wales) can be found here. The UCSB Press Release can be found here. Follow these links to read how this story was reported by: Science Now, the Australian Broadcasting Company, the National Geographic News, The Santa Barbara Independent and The Santa Barbara News-Press and The Telegraph. T.A.F. Long, P.M. Miller, A.D. Stewart and W.R. Rice. 2009. Estimating the heritability of adult female fitness in a locally adapted Drosophila melanogaster population. Journal of Evolutionary Biology. 22: 637-643. Abstract: The heritability of genome-wide fitness that is expected in finite populations is poorly understood, both theoretically and empirically, despit its relevance to many fundamental concepts in evolutionary biology. In this study, we used two independent methds of estimating the heritability of lifetime female fecundity (the predominant female fitness component in this population) in a large, outbred population of Drosophila melanogaster that had adapted to the laboratory environment for over 400 generations. Despite strong directional selection on adult female fecundity, we uncovered high heritability for this trait that cannot be explained by antogonitic pleiotropy with juvenile fitness. The evolutionary significance of this high heritability of lifetime fecundity is discussed. *T.A.F. Long, A.D. Stewart and P.M. Miller. 2009. Potential confounds to an assay of cross-generational fitness benefits of mating and male seminal fluid. Biology Letters. 5: 26-27.* In this review paper, we discusss our concerns regarding the results and conclusions of the paper "Cross-generational fitness benefits of mating and male seminal fluid. 2008. Biology Letters. 4: 6-8." which can be found here. Priest et al.'s response to our review can be found here. *T.A.F. Long and W.R. Rice. 2007. Adult locomotory activity mediates intralocus sexual conflict in a laboratory-adapted population of Drosophila melanogaster.* Proceeding of the Royal Society of London, Series B. 274: 3105-3112. Abstract: The strongest form of intralocus sexual conflict occurs when two conditions are met: (i) there is a positive intersexual genetic correlation for a trait and (ii) the selection gradients on the trait in the two sexes are in opposite directions. Intralocus sexual conflict can constrain the adaptive evolution of both sexes and thereby contribute to a species' 'gender load'. Previous studies of adult lifetime fitness of the same sets of genes expressed in both males and females have established that there is substantial intralocus conflict in the LHM laboratory-adapted population of Drosophila melanogaster. Here, we investigated whether a highly dimorphic trait-adult locomotory activity-contributed substantially to the established intralocus sexual conflict. To measure the selection gradient on activity level, both this trait and adult lifetime fitness were measured under the same environmental conditions to which the flies were adapted. We found significant phenotypic variation in both sexes for adult locomotory activity, and that the selection gradients on this variation were large and in opposite directions in the two sexes. Using hemiclonal analysis to screen 99% of the entire genome, we found abundant genetic variation for adult locomotory activity and showed that this variation occurs on both the X and autosomes. We also established that there is a strong positive intersexual genetic correlation for locomotory activity. These assays revealed that, despite the strong, extant sexual dimorphism for the trait, locomotory activity continues to contribute strongly to intralocus sexual conflict in this population. Note: For electronic supplementary material please click here: T.A.F. Long, R. Montgomerie and A. Chippindale. 2006. Quantifying the gender load: can population crosses reveal interlocus sexual conflict? Philosophical Transactions of the Royal Society of London, Series B. 361: 363-374. Abstract: If interlocus sexual conflict drives the evolution of reproductive characters, then females are expected to be best-defended against (or least sensitive to) the specific manipulative traits of males in their breeding population. However, depending upon the nature of the coevolving signal-receiver system, crosses between different populations of the same species can theoretically lead to a negative or positive impact of foreign males on female fitness. Using a long-term, laboratory-evolved phylogeny of replicate Drosophila melanogaster populations, we show that intersexual coevolution is rapid and leads to interactions that strongly and directly influence female net fitness, mating, and sperm use patterns. The tendency (19/30 crosses) for foreign males to negatively influence female fitness may be interpreted as evidence for either sexually antagonistic coevolution or the disruption of mutualistically coevolved interactions. Rather, we suggest that instances in which female fitness was improved by mating with foreign males may better reveal the extent of sexual conflict, signaling release from the gender load established by antagonistic coevolution. Variation in both female mating rate and male post-copulatory fitness in response to matings between females and local versus foreign males also showed that populations had diverged in a manner consistent with interlocus sexual conflict. This paper was presented at the discussion meeting "Sexual conflic: a new paradigm?", hosted by the Royal Society of London. More information on this event can be found here: *T.A.F. Long and R. Montgomerie. 2005. Ejaculate investment in a promiscuous rodent, Peromyscus maniculatus: effects of population density and social role. Evolutionary Ecology Research.* 8: 345-356. Abstract*: Questions: How does average male investment into ejaculates vary with changing population density (and thus with the risk of sperm competition) in a promiscuous species? Do individual male investment strategies vary with population density? Data Studied: Total testes mass, somatic mass and annual population density for wild-caught male deer mice, Peromyscus maniculatus, collected by snap-trapping over a 23-year period in Algonquin Provincial Park, ON, Canada. Search Methods: We analyzed the relation between mean testes mass and mouse population densities across years. To investigate individual investment patterns, we compared the relation between total testes mass and somatic mass among males for years differing in population density. Conclusions: Average investment into testes was positively correlated with annual population density. An individual's investment into testes depended on both the abundance of rival males and on relative body size, a trait associated with social rank. T.A.F. Long and A. Pischedda 2005. Do female Drosophila melanogaster adaptively bias offspring sex ratios in relation to the age of their mate? Proceedings of the Royal Society of London, Series B.* 272: 1781-1787. Abstract. Modification of offspring sex ratios in response to parental quality is predicted when the long-term fitness returns of sons and daughters differ. One factor that may influence a mother's sex allocation decision is the quality (or attractiveness) of her mate. We investigated whether the sex ratios of offspring produced by female Drosophila melanogaster are biased with respect to the age of the males to which they are mated, and whether there is an adaptive basis for this phenomenon. We found that females mated to old males (13d post-eclosion) initially produced a greater proportion of daughters than did females mated to young males (1d post-eclosion). This pattern does not appear to be due to a systematic difference in the numbers or mortality of the X- and Y-bearing sperm originating from old and young fathers, as the overall sex ratios of all offspring produced from a single copulation did not differ between broods fathered by the two types of males. The sons of older males fared worse in competitive mating assays than did the sons of younger males, while daughters of old and young males were of comparable fitness. These results suggest that there is an adaptive basis for the observed sex ratio modification. Science Now's coverage of this paper can be read here: *T.A.F. Long. 2005. The influence of mating system on the intensity of parent-offspring conflict in primates. Journal of Evolutionary Biology. 18: 509-515.* Abstract: An evolutionary conflict of interest exists between parents and their offspring over the partitioning of parental investment (PI) among siblings. When the direct fitness benefits to offspring of increased PI, outweigh the inclusive fitness costs from lost future sibling fitness, selection should favour the evolution of offspring selfishness over altruism. In theory, this conflict is heightened when females are not strictly monogamous, as current offspring should be less altruistic towards future half-siblings than they would be towards full-siblings. Using data collected on foetal growth rate (representing prenatal PI) in primates, I test the prediction from theory that the resolution of the parent-offspring conflict will be closer to the offspring's evolutionary optima in polyandrous species than in more monandrous species. Using phylogenetic comparative analysis, and controlling for allometry, I show that offspring are able to obtain more PI when the probability of future full-siblings decreases, and that this is most pronounced in taxa where there is the opportunity for direct foetal access to the maternal bloodstream. These results support the hypothesis that the resolution of prenatal PI conflict is influenced by both a species' mating system and by its placental structure. *C. Lewis and T.A.F. Long 2005. Courtship and reproduction in Carybdea sivickisi* (Cnidaria: Cubozoa) Marine Biology.147: 477-483. Abstract*: Courtship and fertilization events in cubozoans have received little attention from biologists, and much of what we know about these processes is based on conjecture or scant anecdotal evidence. I set out to describe these processes in the cubozoan Carybdea sivickisi* by observing mature medusae in vitro. Mature adults engage in courtship during which spermatophores are transferred from the male to the female, who then inserts the gametes into her manubrium. Females accepted multiple spermatophores from multiple males, and only produced one embryo strand. This study also provides evidence that the presence of conspicuous velar spots on the females bell margin is a signal of sexual maturity, and that sexual maturity was not reached in either sex until individuals had a bell diameter of at least 5 mm. Non Refereed Publication Seminal Advances in Sexual Selection. Report on 2003 Biology of Spermatozoa Conference. Inintially published on (now defunct) Biomednet.com. Now located here.