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paco.garcia[at]ebd.csic.es

The evolution of polyandry (female multiple mating)

Publications filtered by: The evolution of polyandry (female multiple mating)

Patterns of paternity skew among polyandrous social insects: What can they tell us about the potential for sexual selection?
Jaffé, R., F. Garcia-Gonzalez, S. P. A. den Boer, L. W. Simmons, & B. Baer. 2012 Patterns of paternity skew among polyandrous social insects: What can they tell us about the potential for sexual selection? Evolution, 66:3778-3788
Abstract

Monogamy results in high genetic relatedness among offspring and thus it is generally assumed to be favored by kin selection. Female multiple mating (polyandry) has nevertheless evolved several times in the social Hymenoptera (ants, bees, and wasps), and a substantial amount of work has been conducted to understand its costs and benefits. Relatedness and inclusive fitness benefits are, however, not only influenced by queen mating frequency but also by paternity skew, which is a quantitative measure of paternity biases among the offspring of polyandrous females.We performed a large-scale phylogenetic analysis of paternity skew across polyandrous social Hymenoptera. We found a general and significant negative association between paternity frequency and paternity skew. High paternity skew, which increases relatedness among colony members and thus maximizes inclusive fitness gains, characterized species with low paternity frequency. However, species with highly polyandrous queens had low paternity skew, with paternity equalized among potential sires. Equal paternity shares among fathers are expected to maximize fitness benefits derived from genetic diversity among offspring. We discuss the potential for postcopulatory sexual selection to influence patterns of paternity in social insects, and suggest that sexual selection may have played a key, yet overlooked role in social evolution.

La evolución de la poliandria
Garcia-Gonzalez, F. 2012 La evolución de la poliandria Investigación y Ciencia 429:9-12
Abstract
Durante siglos se ha considerado que la relación sexual dominante en el mundo animal era la monogamia. Sin embargo, en las últimas décadas, la aplicación sistemática de los análisis de paternidad al estudio del comportamiento ha puesto de manifiesto la amplia presencia de otro fenómeno: la poliandria, el apareamiento de una hembra con varios machos en el transcurso de un mismo episodio reproductivo. Si tomamos como ejemplo uno de los iconos tradicionales de la monogamia, las aves que forman parejas estables, descubrimos que las hembras de más del 70 por ciento de las especies de este grupo copulan con otros machos. Y esto no es una excepción: la poliandria es la norma en un gran número de grupos animales. La poliandria comporta una serie de implicaciones evolutivas de gran calibre y, por ello, su estudio atrae la atención de investigadores en todo el mundo. La consecuencia más importante del comportamiento poliándrico se puede ilustrar con un trabajo clásico que estudió el comportamiento sexual de un grupo de macacos a lo largo de ocho años. El macho dominante del clan consumó el 70 por ciento de las cópulas, mientras que el segundo en el orden de jerarquía apenas participó en el 14 por ciento de ellas. En cambio, el número de descendientes engendrado por el macho dominante resultó ser la mitad que el de su subordinado. De ello se desprende que, en los machos, el éxito en el apareamiento no garantiza el éxito en la procreación cuando impera la poliandria.
Fertilization success and the estimation of genetic variance in sperm competitiveness
Garcia-Gonzalez, F. & Evans, J. P. 2011 Fertilization success and the estimation of genetic variance in sperm competitiveness Evolution, 65: 746-756
Abstract
A key question in sexual selection is whether the ability of males to fertilize eggs under sperm competition exhibits heritable genetic variation. Addressing this question poses a significant problem, however, because a male’s ability to win fertilizations ultimately depends on the competitive ability of rival males. Attempts to partition genetic variance in sperm competitiveness, as estimated from measures of fertilization success, must therefore account for stochastic effects due to the random sampling of rival sperm competitors. In this contribution, we suggest a practical solution to this problem. We advocate the use of simple crossclassified breeding designs for partitioning sources of genetic variance in sperm competitiveness and fertilization success and show how these designs can be used to avoid stochastic effects due to the random sampling of rival sperm competitors. We illustrate the utility of these approaches by simulating various scenarios for estimating genetic parameters in sperm competiveness, and show that the probability of detecting additive genetic variance in this trait is restored when stochastic effects due to the random sampling of rival sperm competitors are controlled. Our findings have important implications for the study of the evolutionary maintenance of polyandry.
Good genes and sexual selection in dung beetles (Onthophagus taurus): Genetic variance in egg-to-adult and adult viability
Garcia-Gonzalez, F. & Simmons, L. W. 2011 Good genes and sexual selection in dung beetles (Onthophagus taurus): Genetic variance in egg-to-adult and adult viability PLoS ONE, 6:e16233
Abstract
Whether species exhibit significant heritable variation in fitness is central for sexual selection. According to good genes models there must be genetic variation in males leading to variation in offspring fitness if females are to obtain genetic benefits from exercising mate preferences, or by mating multiply. However, sexual selection based on genetic benefits is controversial, and there is limited unambiguous support for the notion that choosy or polyandrous females can increase the chances of producing offspring with high viability. Here we examine the levels of additive genetic variance in two fitness components in the dung beetle Onthophagus taurus. We found significant sire effects on egg-to-adult viability and on son, but not daughter, survival to sexual maturity, as well as moderate coefficients of additive variance in these traits. Moreover, we do not find evidence for sexual antagonism influencing genetic variation for fitness. Our results are consistent with good genes sexual selection, and suggest that both pre- and postcopulatory mate choice, and male competition could provide indirect benefits to females.
Male-induced costs of mating for females compensated by offspring viability benefits in an insect
Garcia-Gonzalez, F. & Simmons, L. W. 2010 Male-induced costs of mating for females compensated by offspring viability benefits in an insect Journal of Evolutionary Biology, 23: 2066-2075
Abstract
Sexual conflict facilitates the evolution of traits that increase the reproductive success of males at the expense of components of female fitness. Theory suggests that indirect benefits are unlikely to offset the direct costs to females from antagonistic male adaptations, but empirical studies examining the net fitness pay-offs of the interaction between the sexes are scarce. Here, we investigate whether matings with males that invest intrinsically more into accessory gland tissue undermine female lifetime reproductive success (LRS) in the cricket Teleogryllus oceanicus. We found that females incur a longevity cost of mating that is proportional to the partner’s absolute investment into the production of accessory gland products. However, male accessory gland weight positively influences embryo survival, and harmful ejaculate-induced effects are cancelled out when these are put in the context of female LRS. The direct costs of mating with males that sire offspring with higher viability are thus compensated by direct and possibly indirect genetic benefits in this species.
Selección sexual post-cópula y la evolución de la poliandria. In: Dopazo, H. and Navarro, A. (Eds). Adaptación y Evolución. 150 años después del Origen de las Especies.
Garcia-Gonzalez, F. 2009 Selección sexual post-cópula y la evolución de la poliandria. In: Dopazo, H. and Navarro, A. (Eds). Adaptación y Evolución. 150 años después del Origen de las Especies Sociedad Española de Biología Evolutiva-Obrapropia S. L., Valencia
Abstract

En un gran número de especies las hembras se aparean de manera poliándrica (con varios machos durante un mismo episodio reproductivo). Este comportamiento tiene consecuencias evolutivas de suma importancia, incluyendo que posibilita la continuación de la selección sexual más allá del apareamiento. Por ello, la comprensión del significado adaptativo de la poliandria ha suscitado gran interés entre los biólogos evolutivos. Aquí se exponen, a grandes rasgos, las principales hipótesis que se han sugerido para explicar el apareamiento múltiple femenino desde una perspectiva evolutiva, y se discuten brevemente algunos retos pendientes en este área. Se destaca el hecho de que existen procesos de selección sexual post-cópula que pueden jugar un papel fundamental en la adquisición de beneficios de naturaleza genética por parte de las hembras poliándricas.

Evolutionary reduction in testes size and competitive fertilization success in response to the experimental removal of sexual selection in dung beetles
Simmons, L. W. & Garcia-Gonzalez, F. 2008 Evolutionary reduction in testes size and competitive fertilization success in response to the experimental removal of sexual selection in dung beetles Evolution, 62:2580-2591
Abstract
Sexual selection is thought to favor the evolution of secondary sexual traits in males that contribute to mating success. In species where females mate with more than one male, sexual selection also continues after copulation in the form of sperm competition and cryptic female choice. Theory suggests that sperm competition should favor traits such as testes size and sperm production that increase a male’s competitive fertilization success. Studies of experimental evolution offer a powerful approach for assessing evolutionary responses to variation in sexual selection pressures. Here we removed sexual selection by enforcing monogamy on replicate lines of a naturally polygamous horned beetle, Onthophagus taurus, and monitoring male investment in their testes for 21 generations. Testes size decreased in monogamous lines relative to lines in which sexual selection was allowed to continue. Differences in testes size were dependent on selection history and not breeding regime. Males from polygamous lines also had a competitive fertilization advantage when in sperm competition with males from monogamous lines. Females from polygamous lines produced sons in better condition, and those from monogamous lines increased their sons condition by mating polygamously. Rather than being costly for females, multiple mating appears to provide females with direct and/or indirect benefits. Neither body size nor horn size diverged between our monogamous and polygamous lines. Our data show that sperm competition does drive the evolution of testes size in onthophagine beetles, and provide general support for sperm competition theory.
The relative nature of fertilization success: implications for the study of post-copulatory sexual selection
Garcia-Gonzalez, F. 2008 The relative nature of fertilization success: implications for the study of post-copulatory sexual selection BMC Evolutionary Biology, 8:140
Abstract
Background: The determination of genetic variation in sperm competitive ability is fundamental to distinguish between post-copulatory sexual selection models based on good-genes vs compatible genes. The sexy-sperm and the good-sperm hypotheses for the evolution of polyandry require additive (intrinsic) effects of genes influencing sperm competitiveness, whereas the genetic incompatibility hypothesis invokes non-additive genetic effects. A male's sperm competitive ability is typically estimated from his fertilization success, a measure that is dependent on the ability of rival sperm competitors to fertilize the ova. It is well known that fertilization success may be conditional to genotypic interactions among males as well as between males and females. However, the consequences of effects arising from the random sampling of sperm competitors upon the estimation of genetic variance in sperm competitiveness have been overlooked. Here I perform simulations of mating trials performed in the context of sibling analysis to investigate whether the ability to detect additive genetic variance underlying the sperm competitiveness phenotype is hindered by the relative nature of fertilization success measurements. Results: Fertilization success values render biased sperm competitive ability values. Furthermore, asymmetries among males in the errors committed when estimating sperm competitive abilities are likely to exist as long as males exhibit variation in sperm competitiveness. Critically, random effects arising from the relative nature of fertilization success lead to an underestimation of underlying additive genetic variance in sperm competitive ability. Conclusion: The results show that, regardless of the existence of genotypic interactions affecting the output of sperm competition, fertilization success is not a perfect predictor of sperm competitive ability because of the stochasticity of the background used to obtain fertilization success measures. Random effects need to be considered in the debate over the maintenance of genetic variation in sperm competitiveness, and when testing good-genes and compatible-genes processes as explanations of polyandrous behaviour using repeatability/heritability data in sperm competitive ability. These findings support the notion that the genetic incompatibility hypothesis needs to be treated as an alternative hypothesis, rather than a null hypothesis, in studies that fail to detect intrinsic sire effects on the sperm competitiveness phenotype.
Garcia-Gonzalez, F. 2008 Male genetic quality and the inequality between paternity success and fertilization success: consequences for studies of sperm competition and the evolution of polyandry Evolution, 62:1653-1665
Abstract
Studies of postcopulatory sexual selection typically estimate a male’s fertilization success from his paternity success (P2) calculated at hatching or birth. However, P2 may be affected by differential embryo viability, thereby confounding estimations of true fertilization success (F2). This study examines the effects of variation in the ability of males to influence embryo viability upon the inequality between P2 and F2. It also investigates the consequences of this inequality for testing the hypothesis that polyandrous females accrue viability benefits for their offspring through facilitation of sperm competition (good-sperm model). Simulations of competitive mating trials show that although relative measures of male reproductive success tend to underestimate the strength of underlying good-sperm processes, good-sperm processes can be seriously overestimated using P2 values if males influence the viability of the embryos they sire. This study cautions the interpretation of P2 values as a proxy for fertilization success or sperm competitiveness in studies of postcopulatory sexual selection, and highlights that the good-sperm hypothesis needs empirical support from studies able to identify and separate unequivocally the males’ ability to win fertilizations from their ability to influence the development of embryos.
Paternal indirect genetic effects on offspring viability and the benefits of polyandry
Garcia-Gonzalez, F. & Simmons, L. W. 2007 Paternal indirect genetic effects on offspring viability and the benefits of polyandry Current Biology, 17: 32-36
Abstract
Although females are expected to maximize their reproductive success with only one or a few matings, the females of many species mate with multiple partners. Experimental studies have found evidence for an increase in egg or embryo viability when females mate polyandrously. These studies have been interpreted in the context of genetic-benefit models that propose that multiple mating increases offspring viability because it allows females to select male genotypes that influence viability directly or because it allows females to avoid genetic incompatibility. However, no studies have examined directly the precise mechanisms by which parents influence embryo viability. Using a morphological marker that enabled us to determine paternity and survival of embryos sired by individual male crickets in both sperm competitive and -noncompetitive situations, we show that males inducing high embryo viability enhance the viability of embryos sired by inferior males. These results indicate that paternal effects and interacting phenotypes determine embryo viability. They show that a male’s reproductive success is modified by the interaction between indirect genetic effects of sperm competitors. Importantly, our findings show that the benefits accruing to offspring of multiply mated females need not be transmitted genetically.

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