An Analytical Framework for Estimating Fertilization Bias and the Fertilization Set from Multiple Sperm-Storage Organs

Manier, Mollie K.; Lüpold, Stefan; Pitnick, Scott; Starmer, William T.

doi:10.1086/671782

Cited by 51 publications

(68 citation statements)

References 68 publications

(107 reference statements)

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“…More recent studies have uncovered a common set of sperm precedence mechanisms shared among closely related species of Drosophila , yet a complex scenario of rapid diversification. For example, male sperm characteristics such as differences in sperm length can contribute to sperm advantage, but females can influence sperm utilization through ejection or by controlling the use of sperm for fertilization (Lupold et al 2013; Manier et al 2013a,b,c). …”

mentioning

confidence: 99%

Do Candidate Genes Mediating Conspecific Sperm Precedence Affect Sperm Competitive Ability Within Species? A Test Case in Drosophila

Civetta

Finn

2014

G3 Genes|Genomes|Genetics

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When females mate to multiple males, the last male to mate fathers the majority of progeny. When males of different species inseminate a female, the sperm of the male conspecific to the female is favored in fertilization in a process known as conspecific sperm precedence (CSP). A large number of studies in Drosophila have assayed the genetic basis of sperm competition, with a main focus on D. melanogaster and accessory gland protein genes. Only a few studies have attempted to disentangle the genetic basis of CSP between related species of Drosophila. Although there is no a priori reason to believe that genes influencing intraspecific sperm competitive ability might also mediate conspecific sperm precedence, no study has addressed the question. Here, we test a group of candidate CSP genes between D. simulans and D. mauritiana for their effect on sperm competition in D. melanogaster. The use of P-element insertion lines identified CG14891 gene disruption as the only one causing a significant decrease in second male paternity success relative to wild-type and ebony tester males. The gene disruption affected both sperm displacement and the sperm fertilizing ability. Out of five genes tested using RNA interference, only gene knockdown of CG6864 (Mst89B) significantly reduced the male’s ability to father progeny when second to mate. Our results suggest that CG14891 and CG6864 might have been co-opted from an intraspecies gene function (i.e., sperm competition) into an interspecies avoidance phenotype (i.e., CSP). Alternatively, the dual role of these genes could be a consequence of their pleiotropic roles.

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mentioning

confidence: 99%

Do Candidate Genes Mediating Conspecific Sperm Precedence Affect Sperm Competitive Ability Within Species? A Test Case in Drosophila

Civetta

Finn

2014

G3 Genes|Genomes|Genetics

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“…This pattern of sperm use contrasts starkly with that of Drosophila simulans, in which females may influence relative fertilization success directly even after sperm ejection. In this species, sperm for fertilization derive equally from the spermathecae and SR, and each sperm-storage organ exhibits a significant bias: favoring firstmale sperm in the SR and second-male sperm in the spermathecae, with females able to shift toward one or the other storage organ depending on the mating order of males of differing quality (46,47). Nevertheless, in the present study we also did find genetic variation in female remating intervals and progeny production rates (also see refs.…”

Section: Discussionmentioning

confidence: 99%

Female mediation of competitive fertilization success in Drosophila melanogaster

Lüpold

Pitnick

Berben

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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117

183

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How females store and use sperm after remating can generate postcopulatory sexual selection on male ejaculate traits. Variation in ejaculate performance traits generally is thought to be intrinsic to males but is likely to interact with the environment in which sperm compete (e.g., the female reproductive tract). Our understanding of female contributions to competitive fertilization success is limited, however, in part because of the challenges involved in observing events within the reproductive tract of internally fertilizing species while discriminating among sperm from competing males. Here, we used females from crosses among isogenic lines of Drosophila melanogaster, each mated to two genetically standardized males (the first with green-and the second with red-tagged sperm heads) to demonstrate heritable variation in female remating interval, progeny production rate, sperm-storage organ morphology, and a number of sperm performance, storage, and handling traits. We then used multivariate analyses to examine relationships between this female-mediated variation and competitive paternity. In particular, the timing of female ejection of excess second-male and displaced first-male sperm was genetically variable and, by terminating the process of sperm displacement, significantly influenced the relative numbers of sperm from each male competing for fertilization, and consequently biased paternity. Our results demonstrate that females do not simply provide a static arena for sperm competition but rather play an active and pivotal role in postcopulatory processes. Resolving the adaptive significance of genetic variation in female-mediated mechanisms of sperm handling is critical for understanding sexual selection, sexual conflict, and the coevolution of male and female reproductive traits.cryptic female choice | heritability | sperm ejection

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“…Deviations from such expectations are inconsistent with sperm competition explanations and instead lend support to CFC. For example, Parker et al [86] generated expectations for P 2 based on S 2 , and this approach was later modified for non-normal data 87, 88 and multiple SSOs [89]. Finally, a significant male × female interaction indicates nondirectional CFC, consistent differences across male–female combinations in utilization or fertilization success [90].…”

Section: Demonstrating Cfcmentioning

confidence: 99%

Postmating Female Control: 20 Years of Cryptic Female Choice

Firman

Gasparini

Manier

et al. 2017

Trends in Ecology & Evolution

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309

329

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Cryptic female choice (CFC) represents postmating intersexual selection arising from female-driven mechanisms at or after mating that bias sperm use and impact male paternity share. Although biologists began to study CFC relatively late, largely spurred by Eberhard’s book published 20 years ago, the field has grown rapidly since then. Here, we review empirical progress to show that numerous female processes offer potential for CFC, from mating through to fertilization, although seldom has CFC been clearly demonstrated. We then evaluate functional implications, and argue that, under some conditions, CFC might have repercussions for female fitness, sexual conflict, and intersexual coevolution, with ramifications for related evolutionary phenomena, such as speciation. We conclude by identifying directions for future research in this rapidly growing field.

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An Analytical Framework for Estimating Fertilization Bias and the Fertilization Set from Multiple Sperm-Storage Organs

Cited by 51 publications

References 68 publications

Do Candidate Genes Mediating Conspecific Sperm Precedence Affect Sperm Competitive Ability Within Species? A Test Case in Drosophila

Do Candidate Genes Mediating Conspecific Sperm Precedence Affect Sperm Competitive Ability Within Species? A Test Case in Drosophila

Female mediation of competitive fertilization success in Drosophila melanogaster

Postmating Female Control: 20 Years of Cryptic Female Choice

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