Precopulatory but not postcopulatory male reproductive traits diverge in response to mating system manipulation in Drosophila melanogaster

Published on Dec 1, 2017in Ecology and Evolution2.392
· DOI :10.1002/ECE3.3542
Kristina U. Wensing5
Estimated H-index: 5
(WWU: University of Münster),
Mareike Koppik6
Estimated H-index: 6
(WWU: University of Münster),
Claudia Fricke21
Estimated H-index: 21
(WWU: University of Münster)
: Competition between males creates potential for pre- and postcopulatory sexual selection and conflict. Theory predicts that males facing risk of sperm competition should evolve traits to secure their reproductive success. If those traits are costly to females, the evolution of such traits may also increase conflict between the sexes. Conversely, under the absence of sperm competition, one expectation is for selection on male competitive traits to relax thereby also relaxing sexual conflict. Experimental evolution studies are a powerful tool to test this expectation. Studies in multiple insect species have yielded mixed and partially conflicting results. In this study, we evaluated male competitive traits and male effects on female costs of mating in Drosophila melanogaster after replicate lines evolved for more than 50 generations either under enforced monogamy or sustained polygamy, thus manipulating the extent of intrasexual competition between males. We found that in a setting where males competed directly with a rival male for access to a female and fertilization of her ova polygamous males had superior reproductive success compared to monogamous males. When comparing reproductive success solely in double mating standard sperm competition assays, however, we found no difference in male sperm defense competitiveness between the different selection regimes. Instead, we found monogamous males to be inferior in precopulatory competition, which indicates that in our system, enforced monogamy relaxed selection on traits important in precopulatory rather than postcopulatory competition. We discuss our findings in the context of findings from previous experimental evolution studies in Drosophila ssp. and other invertebrate species.
#1Joanne L. Godwin (UEA: University of East Anglia)H-Index: 5
#2Ramakrishnan Vasudeva (UEA: University of East Anglia)H-Index: 6
Last. Matthew J. G. Gage (UEA: University of East Anglia)H-Index: 41
view all 7 authors...
It is the differences between sperm and eggs that fundamentally underpin the differences between the sexes within reproduction. For males, it is theorized that widespread sperm competition leads to selection for investment in sperm numbers, achieved by minimizing sperm size within limited resources for spermatogenesis in the testis. Here, we empirically examine how sperm competition shapes sperm size, after more than 77 generations of experimental selection of replicate lines under either high o...
27 CitationsSource
#1Claudia Fricke (UEA: University of East Anglia)H-Index: 21
#2Tracey Chapman (UEA: University of East Anglia)H-Index: 56
Sperm competition is pervasive and fundamental to determining a male’s overall fitness. Sperm traits and seminal fluid proteins (Sfps) are key factors. However, studies of sperm competition may often exclude females that fail to remate during a defined period. Hence, the resulting datasets contain fewer data from the potentially fittest males that have most success in preventing female remating. It is also important to consider a male’s reproductive success before entering sperm competition, whi...
8 CitationsSource
#1Tejinder Singh Chechi (Indian Institute of Science Education and Research, Mohali)H-Index: 1
#2Zeeshan Ali Syed (Indian Institute of Science Education and Research, Mohali)H-Index: 3
Last. Nagaraj Guru Prasad (Indian Institute of Science Education and Research, Mohali)H-Index: 18
view all 3 authors...
Sperm competition theory predicts that with increase in sperm competition, males either invest more in reproductive organ(s) and/or improve ejaculate investment. We test this idea using experimental evolution in Drosophila melanogaster. We maintained replicate populations of Drosophila melanogaster under male (M) and female (F) biased sex ratio regimes for more than a hundred generations with the result that males from the M regime evolved higher sperm competitive abilities relative to males fro...
9 CitationsSource
#1Brian Hollis (EPFL: École Polytechnique Fédérale de Lausanne)H-Index: 9
#2Laurent Keller (UNIL: University of Lausanne)H-Index: 94
Last. Tadeusz J. Kawecki (UNIL: University of Lausanne)H-Index: 42
view all 3 authors...
Explanations for the evolution of delayed maturity usually invoke trade-offs mediated by growth, but processes of reproductive maturation continue long after growth has ceased. Here, we tested whether sexual selection shapes the rate of posteclosion maturation in the fruit fly Drosophila melanogaster. We found that populations maintained for more than 100 generations under a short generation time and polygamous mating system evolved faster posteclosion maturation and faster egg-to-adult developm...
8 CitationsSource
#1Kathryn B. McNamaraH-Index: 14
Last. Leigh W. SimmonsH-Index: 98
view all 6 authors...
Sperm competition risk and intensity can select for adaptations that increase male fertilisation success. Evolutionary responses are examined typically by generating increased strength of sexual selection via direct manipulation of female mating rates (by enforcing monandry or polyandry) or by alteration of adult sex ratios. Despite being a model species for sexual selection research, the effect of sexual selection intensity via adult sex-ratio manipulation on male investment strategies has not ...
6 CitationsSource
#1Ralph Dobler (University of Tübingen)H-Index: 8
#2Klaus Reinhardt (University of Tübingen)H-Index: 29
Sperm-competition success (SCS) is seen as centrally important for evolutionary change: superior fathers sire superior sons and thereby inherit the traits that make them superior. Additional hypotheses, that phenotypic plasticity in SCS and sperm ageing explain variation in paternity, are less considered. Even though various alleles have individually been shown to be correlated with variation in SCS, few studies have addressed the heritability, or evolvability, of overall SCS. Those studies that...
6 CitationsSource
#1Douglas M. BatesH-Index: 38
#2Martin MächlerH-Index: 13
Last. Steven C. WalkerH-Index: 17
view all 4 authors...
Maximum likelihood or restricted maximum likelihood (REML) estimates of the parameters in linear mixed-effects models can be determined using the lmer function in the lme4 package for R. As for most model-fitting functions in R, the model is described in an lmer call by a formula, in this case including both fixed- and random-effects terms. The formula and data together determine a numerical representation of the model from which the profiled deviance or the profiled REML criterion can be evalua...
31.8k CitationsSource
#1Xavier A. Harrison (ZSL: Zoological Society of London)H-Index: 18
Overdispersion is a common feature of models of biological data, but researchers often fail to model the excess variation driving the overdispersion, resulting in biased parameter estimates and standard errors. Quantifying and modeling overdispersion when it is present is therefore critical for robust biological inference. One means to account for overdispersion is to add an observation-level random effect (OLRE) to a model, where each data point receives a unique level of a random effect that c...
165 CitationsSource
#1Renée C. Firman (UWA: University of Western Australia)H-Index: 19
#2Francisco Garcia-Gonzalez (CSIC: Spanish National Research Council)H-Index: 25
Last. Leigh W. Simmons (UWA: University of Western Australia)H-Index: 98
view all 7 authors...
Theory assumes that postcopulatory sexual selection favors increased investment in testes size because greater numbers of sperm within the ejaculate increase the chance of success in sperm competition, and larger testes are able to produce more sperm. However, changes in the organization of the testes tissue may also affect sperm production rates. Indeed, recent comparative analyses suggest that sperm competition selects for greater proportions of sperm-producing tissue within the testes. Here, ...
29 CitationsSource
#1Laura K. Sirot (College of Wooster)H-Index: 21
#2Alex Wong (Carleton University)H-Index: 25
Last. Mariana F. Wolfner (Cornell University)H-Index: 79
view all 4 authors...
Both sexes benefit from successful reproduction, but the different reproductive strategies adopted by males and females may result in differential costs and benefits. This can result in sexual conflict before, during, and after mating. Conflict in the more familiar form of competition can also occur between females and between males, with the latter situation including interejaculate competition. Of the many “weapons” in these conflicts and competitions, this article focuses on the seminal fluid...
97 CitationsSource
Cited By5
#1Eric Desjardins (UWO: University of Western Ontario)H-Index: 5
#2Joachim KurtzH-Index: 37
Last. S. Helene Richter (Animal Welfare Institute)H-Index: 16
view all 5 authors...
#1Mital A (Linköping University)H-Index: 1
#2Manaswini SarangiH-Index: 2
Last. Amitabh JoshiH-Index: 26
view all 5 authors...
The role of sexual selection in mediating levels of sexual conflict has been demonstrated in a number of experimental evolution studies on Drosophila sp. where the level of competition among males for fertilization success was under direct selection. Here we report that selection for a short development time and early age at reproduction can lead to inadvertent changes in levels of sexual selection in D. melanogaster populations, affecting reproductive competition experienced by males. We demons...
#1Alberto Civetta (University of Winnipeg)H-Index: 21
#2José M. Ranz (UCI: University of California, Irvine)H-Index: 19
Females of many different species often mate with multiple males, creating opportunities for competition among their sperm. Although originally unappreciated, sperm competition is now considered a central form of post-copulatory male-male competition that biases fertilization. Assays of differences in sperm competitive ability between males, and interactions between females and males, have made it possible to infer some of the main mechanism of sperm competition. Nevertheless, classical genetic ...
23 CitationsSource
#1Brian Hollis (EPFL: École Polytechnique Fédérale de Lausanne)H-Index: 9
#2Mareike Koppik (WWU: University of Münster)H-Index: 6
Last. Laurent Keller (UNIL: University of Lausanne)H-Index: 94
view all 9 authors...
In many animals, females respond to mating with changes in physiology and behavior that are triggered by molecules transferred by males during mating. In Drosophila melanogaster, proteins in the seminal fluid are responsible for important female postmating responses, including temporal changes in egg production, elevated feeding rates and activity levels, reduced sexual receptivity, and activation of the immune system. It is unclear to what extent these changes are mutually beneficial to females...
32 CitationsSource
#1David C. S. Filice (WLU: Wilfrid Laurier University)H-Index: 4
#2Tristan A. F. Long (WLU: Wilfrid Laurier University)H-Index: 13
In Drosophila melanogaster, males engage in both extensive pre- and post-copulatory competition for the opportunity to mate with females and subsequently sire offspring. The selection pressure for ...
3 CitationsSource