scholarly journals Female × male and male × male interactions have limited influence on competitive fertilization inDrosophila melanogaster

2019 ◽  
Author(s):  
Stefan Lüpold ◽  
Jonathan Bradley Reil ◽  
Mollie K. Manier ◽  
Valérian Zeender ◽  
John M. Belote ◽  
...  

AbstractHow males and females contribute to joint reproductive success has been a long-standing question in sexual selection. Under postcopulatory sexual selection (PSS), paternity success is predicted to derive from complex interactions among females engaging in cryptic female choice and males engaging in sperm competition. Such interactions have been identified as potential sources of genetic variation in sexually selected traits but are also expected to inhibit trait diversification. To date, studies of interactions between females and competing males have focused almost exclusively on genotypes and not phenotypic variation in sexually selected traits. Here, we characterize within- and between-sex interactions inDrosophila melanogasterusing isogenic lines with heritable variation in both male and female traits known to influence competitive fertilization. We found surprisingly few genotypic interaction effects on various stages of PSS such as female remating interval, copulation duration, sperm transfer, or sperm storage. Only the timing of female sperm ejection depended on female × male genotypic interactions. By contrast, several reproductive events, including sperm transfer, female sperm ejection and sperm storage, were explained by two- and three-way interactions among sex-specific phenotypes. We also documented complex interactions between the lengths of competing males’ sperm and the female seminal receptacle, which are known to have experienced rapid female-male co-diversification. Our results highlight the non-independence of sperm competition and cryptic female choice and demonstrate that complex interactions between the sexes do not limit the ability of multivariate systems to respond to directional sexual selection.Significance statementFor species with internal fertilization and female promiscuity, postcopulatory sexual selection (PSS) is believed to depend, in part, on complex interactions between rival males and between the sexes. Although little investigated, clarifying such interactions is critical as they may limit the efficacy of PSS in the diversification of reproductive traits (e.g., ejaculate biochemistry and sperm, genitalia and female reproductive tract morphology). Here, we resolve how sex-specific traits and their interactions contribute to key reproductive events and outcomes related to competitive fertilization success, including traits known to have experienced rapid diversification. Our results provide novel insights into the operation and complexity of PSS and demonstrate that the processes of sperm competition and cryptic female choice are not independent selective forces.

Author(s):  
Patricia L.R. Brennan ◽  
Dara N. Orbach

The field of post-copulatory sexual selection investigates how female and male adaptations have evolved to influence the fertilization of eggs while optimizing fitness during and after copulation, when females mate with multiple males. When females are polyandrous (one female mates with multiple males), they may optimize their mating rate and control the outcome of mating interactions to acquire direct and indirect benefits. Polyandry may also favor the evolution of male traits that offer an advantage in post-copulatory male-male sperm competition. Sperm competition occurs when the sperm, seminal fluid, and/or genitalia of one male directly impacts the outcome of fertilization success of a rival male. When a female mates with multiple males, she may use information from a number of traits to choose who will sire her offspring. This cryptic female choice (CFC) to bias paternity can be based on behavioral, physiological, and morphological criteria (e.g., copulatory courtship, volume and/or composition of seminal fluid, shape of grasping appendages). Because male fitness interests are rarely perfectly aligned with female fitness interests, sexual conflict over mating and fertilization commonly occur during copulatory and post-copulatory interactions. Post-copulatory interactions inherently involve close associations between female and male reproductive characteristics, which in many species potentially include sperm storage and sperm movement inside the female reproductive tract, and highlight the intricate coevolution between the sexes. This coevolution is also common in genital morphology. The great diversity of genitalia among species is attributed to sexual selection. The evolution of genital attributes that allow females to maintain reproductive autonomy over paternity via cryptic female choice or that prevent male manipulation and sexual control via sexually antagonistic coevolution have been well documented. Additionally, cases where genitalia evolve through intrasexual competition are well known. Another important area of study in post-copulatory sexual selection is the examination of trade-offs between investments in pre-copulatory and post-copulatory traits, since organisms have limited energetic resources to allocate to reproduction, and securing both mating and fertilization is essential for reproductive success.


2008 ◽  
Vol 86 (11) ◽  
pp. 1244-1251 ◽  
Author(s):  
Ronald Chase ◽  
Emily Darbyson

The sperm storage organ of terrestrial gastropod molluscs is implicated in sexual selection because it has a complex structure and it functions in a context of intense sperm competition. Received sperm are stored in spermathecal tubules. In our sample using the brown garden snail ( Cornu aspersum (Müller, 1774)) (n = 58), the mean number of tubules per animal was 16, with lengths ranging from ≤40 to 2480 μm. A hereditary influence on tubule number was indicated by clutch-dependent variations. From histological sections, we counted the spermatozoa that were present in the tubules of ex-virgin snails 1, 2, 4, and 8 weeks after mating (n = 40). Sperm were distributed, on average, across 75% of the tubules in individual snails, thus contradicting one proposed mechanism for cryptic female choice. The total number of sperm declined 66% over 8 weeks, with the largest losses incurred by sperm in the lumens of the tubules and sperm gathered in clusters. By contrast, in the same period, the numbers of sperm that were in contact with the walls of the tubules remained relatively stable. These data imply that sperm survive best when attached to the epithelial wall, either because they derive nutrition from the epithelium or because they use the epithelium as an anchor.


Author(s):  
Leigh W. Simmons

Darwin viewed sexual selection as a process that ended with mate acquisition, assuming that females are fundamentally monogamous, mating with just one male. ‘Sexual selection after mating’, however, shows this assumption to be false. Sexual selection continues long after the physical act of mating is over, as sperm compete inside a female’s reproductive tract and females bias the paternity of their young by selectively using sperm from particular males. Multiple mating by females has turned out to be ubiquitous across animal taxa. The far-reaching evolutionary consequences of sperm competition and cryptic female choice for the evolution of reproductive traits are examined, from the gametes themselves to the adult organisms producing them.


2014 ◽  
Vol 281 (1797) ◽  
pp. 20142050 ◽  
Author(s):  
Dean M. Castillo ◽  
Leonie C. Moyle

Sexual selection and sexual conflict are considered important drivers of speciation, based on both theoretical models and empirical correlations between sexually selected traits and diversification. However, whether reproductive isolation between species evolves directly as a consequence of intrapopulation sexual dynamics remains empirically unresolved, in part because knowledge of the genetic mechanisms (if any) connecting these processes is limited. Here, we provide evidence of a direct mechanistic link between intraspecies sexual selection and reproductive isolation. We examined genes with known roles in intraspecific sperm competition (ISC) in D. melanogaster and assayed their impact on conspecific sperm precedence (CSP). We found that two such genes ( Acp36DE and CG9997 ) contribute to both offensive sperm competition and CSP; null/knockdown lines both had lower competitive ability against D. melanogaster conspecifics and were no longer able to displace heterospecific D. simulans sperm in competitive matings. In comparison, Sex Peptide ( Acp70A )—another locus essential for ISC—does not contribute to CSP. These data indicate that two loci important for sperm competitive interactions have an additional role in similar interactions that enforce post-mating reproductive isolation between species, and show that sexual selection and sexual isolation can act on the same molecular targets in a gene-specific manner.


2021 ◽  
Vol 18 (1) ◽  
Author(s):  
Lenka Sentenská ◽  
Aileen Neumann ◽  
Yael Lubin ◽  
Gabriele Uhl

Abstract Background Mating generally occurs after individuals reach adulthood. In many arthropods including spiders, the adult stage is marked by a final moult after which the genitalia are fully developed and functional. In several widow spider species (genus Latrodectus), however, immature females may mate a few days before they moult to adulthood, i.e. in their late-subadult stage. While the “adult” mating typically results in cannibalism, males survive the “immature” mating. During both “immature” and “adult” matings, males leave parts of their paired copulatory organs within female genitalia, which may act as mating plugs. To study potential costs and benefits of the two mating tactics, we investigated female genital morphology of the brown widow spider, L. geometricus. Light microscopy, histology and micro-computed tomography of early-subadult, late-subadult and adult females were conducted to determine the overall pattern of genital maturation. We compared genitalia of mated late-subadult and adult females to reveal potential differences in the genitalic details that might indicate differential success in sperm transfer and different environments for sperm storage and sperm competition. Results We found that the paired sperm storage organs (spermathecae) and copulatory ducts are developed already in late-subadult females and host sperm after immature mating. However, the thickness of the spermathecal cuticle and the staining of the secretions inside differ significantly between the late-subadult and adult females. In late-subadult females mating plugs were found with higher probability in both spermathecae compared to adult females. Conclusions Sperm transfer in matings with late-subadult females follows the same route as in matings with adult females. The observed differences in the secretions inside the spermathecae of adult and late-subadult females likely reflect different storage conditions for the transferred sperm which may lead to a disadvantage under sperm competition if the subadult female later re-mates with another male. However, since males mating with late-subadult females typically transfer sperm to both spermathecae they might benefit from numerical sperm competition as well as from monopolizing access to the female sperm storage organs. The assessment of re-mating probability and relative paternity will clarify the costs and benefits of the two mating tactics in light of these findings.


2018 ◽  
Vol 285 (1883) ◽  
pp. 20180836 ◽  
Author(s):  
Jukka Kekäläinen ◽  
Jonathan P. Evans

‘Sperm competition’—where ejaculates from two or more males compete for fertilization—and ‘cryptic female choice’—where females bias this contest to suit their reproductive interests—are now part of the everyday lexicon of sexual selection. Yet the physiological processes that underlie these post-ejaculatory episodes of sexual selection remain largely enigmatic. In this review, we focus on a range of post-ejaculatory cellular- and molecular-level processes, known to be fundamental for fertilization across most (if not all) sexually reproducing species, and point to their putative role in facilitating sexual selection at the level of the cells and gametes, called ‘gamete-mediated mate choice’ (GMMC). In this way, we collate accumulated evidence for GMMC across different mating systems, and emphasize the evolutionary significance of such non-random interactions among gametes. Our overall aim in this review is to build a more inclusive view of sexual selection by showing that mate choice often acts in more nuanced ways than has traditionally been assumed. We also aim to bridge the conceptual divide between proximal mechanisms of reproduction, and adaptive explanations for patterns of non-random sperm–egg interactions that are emerging across an increasingly diverse array of taxa.


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