scholarly journals Post-Insemination Selection Dominates Pre-Insemination Selection in Driving Rapid Evolution of Male Competitive Ability

2021 ◽  
Author(s):  
Katja R Kasimatis ◽  
Megan J Moerdyk-Schauwecker ◽  
Ruben Lancaster ◽  
Alexander Smith ◽  
John H Willis ◽  
...  

Sexual reproduction is a complex process that contributes to differences between the sexes and divergence between species. From a male's perspective, sexual selection can optimize reproductive success by acting on the variance in mating success (pre-insemination selection) as well as the variance in fertilization success (post-insemination selection). The balance between pre- and post-insemination selection has not yet been investigated using a strong hypothesis-testing framework that directly quantifies the effects of post-insemination selection on the evolution of reproductive success. Here we use experimental evolution of a uniquely engineered genetic system that allows sperm production to be turned off and on in obligate male-female populations of Caenorhabditis elegans. We show that enhanced post-insemination competition increases the efficacy of selection and surpasses pre-insemination sexual selection in driving a polygenic response in male reproductive success. We find that after 30 generations post-insemination selection increased male reproductive success by an average of 5- to 7-fold. Contrary to expectation, enhanced pre-insemination competition hindered selection and slowed the rate of evolution. Furthermore, we found that post-insemination selection resulted in a strong polygenic response at the whole-genome level. Our results demonstrate that post-insemination sexual selection plays a critical role in the rapid optimization of male reproductive fitness. Therefore, explicit consideration should be given to post-insemination dynamics when considering the population effects of sexual selection.

Parasitology ◽  
2014 ◽  
Vol 141 (7) ◽  
pp. 934-939
Author(s):  
D. ANDREOU ◽  
D. P. BENESH

SUMMARYSimultaneous hermaphrodites maximize their fitness by optimizing their investment into male or female functions. Allocation of resources to male function (tissues, traits, and/or behaviours increasing paternity) is predicted to increase as density, and the associated level of sperm competition, increases. We tested whether the simultaneous hermaphroditic cestode Schistocephalus solidus uses cues of potential partner densities in its fish intermediate host to improve its male reproductive success in the final host. We had two worms, one originating from a multiple infection in the fish intermediate host and one from a single infection, sequentially compete to fertilize the eggs of a third worm. The fertilization rates of the two competitors nearly always differed from the 50–50 null expectation, sometimes considerably, implying there was a ‘winner’ in each experimental competition. However, we did not find a significant effect of density in the fish host (single vs multiple) or mating order on paternity. Additional work will be needed to identify the traits and environmental conditions that explain the high variance in male reproductive success observed in this experiment.


eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Jeroen NA Hoffer ◽  
Janine Mariën ◽  
Jacintha Ellers ◽  
Joris M Koene

Sexual selection is generally predicted to act more strongly on males than on females. The Darwin-Bateman paradigm predicts that this should also hold for hermaphrodites. However, measuring this strength of selection is less straightforward when both sexual functions are performed throughout the organism’s lifetime. Besides, quantifications of sexual selection are usually done during a short time window, while many animals store sperm and are long-lived. To explore whether the chosen time frame affects estimated measures of sexual selection, we recorded mating success and reproductive success over time, using a simultaneous hermaphrodite. Our results show that male sexual selection gradients are consistently positive. However, an individual’s female mating success seems to negatively affect its own male reproductive success, an effect that only becomes visible several weeks into the experiment, highlighting that the time frame is crucial for the quantification and interpretation of sexual selection measures, an insight that applies to any iteroparous mating system.


2019 ◽  
Vol 15 (5) ◽  
pp. 20190057
Author(s):  
Austin P. Dreyer ◽  
Alexander W. Shingleton

For most arthropod species, male genital size is relatively implastic in response to variation in developmental nutrition, such that the genitals in large well-fed males are similar in size to those in small poorly-fed males. In Drosophila melanogaster, reduced nutritional plasticity of the male genitalia is a consequence of low insulin sensitivity through a tissue-specific reduction in the expression of FOXO , a negative growth regulator . Despite an understanding of the proximate developmental mechanisms regulating organ size, the ultimate evolutionary mechanisms that may have led to reduced FOXO expression in the genitalia have not been fully elucidated. Here we show that restoring FOXO activity in the developing genitalia reduces the male genital size and decreases various aspects of male reproductive success. These data support the hypothesis that sexual selection has acted on the male genitalia to limit their nutritional plasticity through a reduction in FOXO expression, linking proximate with ultimate mechanisms of genital evolution.


The Auk ◽  
2004 ◽  
Vol 121 (3) ◽  
pp. 788-795
Author(s):  
Bruce E. Byers ◽  
Herman L. Mays ◽  
Ian R. K. Stewart ◽  
David F. Westneat

Abstract A monogamous mating system that includes extrapair fertilization can potentially generate higher variability in male reproductive success than monogamy without extrapair fertilization. That increased variability could provide a correspondingly higher opportunity for sexual selection and, thus, for the origin and persistence of sexual dimorphism in monogamous species. To determine whether extrapair fertilization enhanced the opportunity for sexual selection in a sexually dimorphic, monogamous bird species, we used microsatellite DNA typing to assess the prevalence of extrapair fertilization and its effect on variation in male reproductive success in a population of Chestnut-sided Warblers (Dendroica pensylvanica). We found that the level of extrapair fertilization in our study population was at the upper end of the range reported for bird populations (47% of nestlings had extrapair fathers; 61% of broods contained extrapair offspring). We also discovered that almost all extrapair offspring were sired by paired males resident on nearby territories. In addition, we found that variation in male reproductive success was substantially higher than variation in female reproductive success, and that extrapair fertilizations made a significant contribution to variation in male reproductive success. Together, those findings suggest that extrapair fertilization creates an opportunity for sexual selection on male traits in this population.


Author(s):  
Darryl Gwynne

Cyphoderris strepitans Morris and Gwynne is a common species of nocturnal insect in many sagebrush areas within Grand Tetons and Yellowstone National Parks. It is a primitive orthopteran group, a relict of the ancient family Haglidae. Only five species in three genera are currently known (Morris and Gwynne 1978, Storozhenko 1980). Males produce a calling song by rubbing their forewings together. Females are attracted to male song; during mating the female feeds on the tissues of the male's fleshy underwings. Virgin and non-virgin males can, therefore, be distinguished by examining their underwings. At the end of mating the male transfers a large proteinaceous spermatophore which the female also consumes. The main objective of this study has been to investigate the role and consequences of the male investment in his underwings and spermatophore (see Morris and Gwynne 1979). Female katydids use spermatophore proteins for egg production (Gwynne and Toalson unpublished) so these nutrients can be regarded as an important male investment likely to influence patterns of sexual selection within this group. Trivers (1972) outlined the theory of parental investment and its influence on sexual selection. Females, because they produce fewer larger gametes (eggs) are usually the limiting sex for the males which have a relatively large number of small gametes (sperm). As a result, males are predicted to maximize reproductive success by competing with each other to inseminate as many females as possible. Females, because they are limited by their fewer gametes will not gain by competing for copulations. Instead they should enhance reproductive success by being selective about which males fertilize their eggs. Sexual selection should, therefore, be stronger on males since competition for mates should produce a greater variance in the reproductive success of this sex (i.e., some males obtain few or no mates while others mate frequently). Males can offset the initial disparity of investment in gametes by investing parentally via paternal care of eggs or offspring or, as in many insects, by feeding the female with prey items or glandular products (Thornhill 1976). These sorts of male investments should decrease the variance in reproductive success of these males because the males are more "female like" in their reproductive strategy i.e., competing less because they reduce the number of potential copulations engaged in due to the large nutrient investment in each copulation. In orthopterans such as Cyphoderris where females feed on male-produced nutrients the following predictions emerge: (1) females should select a mate who is likely to provide more of the nutrient; (2) as mentioned above, the variance in male reproductive success should be low; few males should go unmated. Previous work in Grand Teton National Park has indicated that females may prefer Cyphoderris males who can supply more nutrients. Significantly more virgin males are mated than non-virgins (Morris and Gwynne 1979). Virgins are likely to be a better mate choice for females since they have not only more wing material but also would have large reproductive accessory glands capable of producing a full sized spermatophore. The main purpose of this season's work was to investigate the variance in reproductive success of males. An effort was also made to further collect information on the distribution of C. strepitans in and around Grand Teton and Yellowstone national parks. This information is presented first. (* Erratum: pp. 51 and 52 should be 56 and 57)


Cells ◽  
2022 ◽  
Vol 11 (2) ◽  
pp. 231
Author(s):  
Melissah Rowe ◽  
Annabel van Oort ◽  
Lyanne Brouwer ◽  
Jan T. Lifjeld ◽  
Michael S. Webster ◽  
...  

Sperm competition is thought to impose strong selection on males to produce competitive ejaculates to outcompete rival males under competitive mating conditions. Our understanding of how different sperm traits influence fertilization success, however, remains limited, especially in wild populations. Recent literature highlights the importance of incorporating multiple ejaculate traits and pre-copulatory sexually selected traits in analyses aimed at understanding how selection acts on sperm traits. However, variation in a male’s ability to gain fertilization success may also depend upon a range of social and ecological factors that determine the opportunity for mating events both within and outside of the social pair-bond. Here, we test for an effect of sperm quantity and sperm size on male reproductive success in the red-back fairy-wren (Malurus melanocephalus) while simultaneously accounting for pre-copulatory sexual selection and potential socio-ecological correlates of male mating success. We found that sperm number (i.e., cloacal protuberance volume), but not sperm morphology, was associated with reproductive success in male red-backed fairy-wrens. Most notably, males with large numbers of sperm available for copulation achieved greater within-pair paternity success. Our results suggest that males use large sperm numbers as a defensive strategy to guard within-pair paternity success in a system where there is a high risk of sperm competition and female control of copulation. Finally, our work highlights the importance of accounting for socio-ecological factors that may influence male mating opportunities when examining the role of sperm traits in determining male reproductive success.


2004 ◽  
Vol 164 (4) ◽  
pp. E83-E89 ◽  
Author(s):  
Michael J. Wade ◽  
Stephen M. Shuster

2020 ◽  
Author(s):  
S. Mark Wainwright ◽  
Cláudia C. Mendes ◽  
Aashika Sekar ◽  
Benjamin Kroeger ◽  
Josephine E.E.U. Hellberg ◽  
...  

AbstractSeminal fluid plays an essential role in promoting male reproductive success and modulating female physiology and behaviour. In the fruit fly, Drosophila melanogaster, Sex Peptide (SP) is the best-characterised protein mediator of these effects. It is secreted from the paired male accessory glands (AGs), which, like the mammalian prostate and seminal vesicles, generate most of the seminal fluid contents. After mating, SP binds to spermatozoa and is retained in the female sperm storage organs. It is gradually released by proteolytic cleavage and induces several long-term post-mating responses including ovulation, elevated feeding and reduced receptivity to remating, primarily signalling through the SP receptor (SPR). Here, we demonstrate a previously unsuspected SPR-independent function for SP. We show that, in the AG lumen, SP and secreted proteins with membrane-binding anchors are carried on abundant, large neutral lipid-containing microcarriers, also found in other SP-expressing Drosophila species. These microcarriers are transferred to females during mating, where they rapidly disassemble. Remarkably, SP is a key assembly factor for microcarriers and is also required for the female disassembly process to occur normally. Males expressing non-functional SP mutant proteins that affect SP’s binding to and release from sperm in females also do not produce normal microcarriers, suggesting that this male-specific defect contributes to the resulting widespread defects in ejaculate function. Our data therefore reveal a novel role for SP in formation of seminal macromolecular assemblies, which may explain the presence of SP in Drosophila species, which lack the signalling functions seen in D. melanogaster.Significance StatementSeminal fluid plays a critical role in reprogramming female physiology and behaviour to promote male reproductive success. We show in the fruit fly that specific seminal proteins, including the archetypal ‘female-reprogramming’ molecule Sex Peptide, are stored in male seminal secretions in association with large neutral lipid-containing microcarriers, which rapidly disperse in females. Related structures are also observed in other Sex Peptide-expressing Drosophila species. Males lacking Sex Peptide have structurally defective microcarriers, leading to abnormal cargo loading and transfer to females. Our data reveal that this key signalling molecule in Drosophila seminal fluid is also a microcarrier assembly factor that controls transfer of other seminal factors, and that this may be a more evolutionarily ancient role of this protein.


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