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Sexual conflict and male-female coevolution in the fruit fly
Umeå University, Faculty of Science and Technology, Ecology and Environmental Science.
2006 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Harmony and cooperation was for long believed to dominate sexual interactions. This view slowly started to change 25 years ago and is today replaced with a view where males and females act based on what is best from a costs-benefits perspective. When sex specific costs and benefits differ, concerning reproductive decision influenced by both sexes, sexual conflict will occur. The basis for discordant reproductive interests between the sexes is that males produce many small gametes, while females’ produce few and large gametes. One result of this difference is that the optimal mating rate differs between the sexes. Males, with their many small sperm, maximize their reproductive output by mating with many females, while females often do best by not mating more frequently than to fertilize their eggs, since mating often entails a cost. Sexual conflict over mating is thus an important factor shaping the interactions between the sexes. In this thesis I study this and related conflicts between the sexes, using mathematical models, fruit flies and comparative methods. Mathematical modelling was used to explore how males and females may coevolve under sexual conflict over mating. This model shows that sexual conflict over mating results in the evolution of costly female mate choice, in terms high resistance to matings, and costly exaggerated male sexual traits, aimed to manipulate females into mating. A key assumption in this model is that males which females find attractive also are more harmful to females. This assumption was tested by housing fruit fly females with either attractive or unattractive males. Females kept with attractive males were courted and mated more, and suffered a 16 percent reduction in lifetime offspring production. In another study I measured genetic variation in two antagonistic male traits used to compete over females; offence - a male’s ability to acquire new mates and supplant stored sperm, and defence - a male’s ability to induce fidelity in his mates and prevent sperm displacement when remating occurs. Independent additive genetic variation and positive selection gradients were found for both these traits, indicating an ongoing arms race between these male antagonistic traits. This arms race also had a negative impact on females, since high values of offence compromised female fitness. Genetic variation in female ability to withstand male harm was also tested for and found, indicating that females evolve counter adaptations to reduce the effect of harmful male traits. Finally, the proposed link between sexual conflict and speciation was tested. Theory suggests that perpetual sexual arms races will cause allopatric populations to evolve along different evolutionary trajectories, resulting in speciation. This theory was tested using comparative methods by contrasting the number of extant species in taxa with high and low opportunity for sexual conflict. The study showed that taxa with high opportunity for sexual conflict, on average, has four times as many species as those with low opportunity, supporting that sexual conflict is a key process in speciation.

Place, publisher, year, edition, pages
Umeå: Ekologi, miljö och geovetenskap , 2006. , 22 p.
Keyword [en]
cryptic male mate choice, Drosophila melanogaster, female mate choice, multiple mating, sexual conflict, sexually antagonistic coevolution, sexual selection, speciation, sperm competition
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:umu:diva-735ISBN: 91-7264-055-3 (print)OAI: oai:DiVA.org:umu-735DiVA: diva2:144360
Public defence
2006-04-20, KB3 A9, KBC-huset, Umeå, 10:00
Opponent
Supervisors
Available from: 2006-03-30 Created: 2006-03-30Bibliographically approved
List of papers
1. The evolution of female mate choice by sexual conflict
Open this publication in new window or tab >>The evolution of female mate choice by sexual conflict
2001 In: Proceedings of the Royal Society of London Series B, ISSN 0080-4649, Vol. 268, no 1466, 531-539 p.Article in journal (Refereed) Published
Identifiers
urn:nbn:se:umu:diva-5010 (URN)
Available from: 2006-03-30 Created: 2006-03-30Bibliographically approved
2. Fitness effects of female mate choice: preferred males are detrimental for Drosophila melanogaster females
Open this publication in new window or tab >>Fitness effects of female mate choice: preferred males are detrimental for Drosophila melanogaster females
2003 In: Journal of Evolutionary Biology, ISSN 1010-061X, Vol. 16, no 5, 797-811 p.Article in journal (Refereed) Published
Identifiers
urn:nbn:se:umu:diva-5011 (URN)
Available from: 2006-03-30 Created: 2006-03-30Bibliographically approved
3. Assessing the potential for an ongoing arms race within and between the sexes: selection and heritable variation
Open this publication in new window or tab >>Assessing the potential for an ongoing arms race within and between the sexes: selection and heritable variation
2005 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 59, no 7, 1540-1551 p.Article in journal (Refereed) Published
Abstract [en]

In promiscuous species, sexual selection generates two opposing male traits: offense (acquiring new mates and supplanting stored sperm) and defense (enforcing fidelity on one's mates and preventing sperm displacement when this fails). Coevolution between these traits requires both additive genetic variation and associated natural selection. Previous work with Drosophila melanogaster found autosomal genetic variation for these traits among inbred lines from a mixture of populations, but only nonheritable genetic variation was found within a single outbred population. These results do not support ongoing antagonistic coevolution between offense and defense, nor between either of these male traits and female reproductive characters. Here we use a new method (hemiclonal analysis) to study genomewide genetic variation in a large outbred laboratory population of D. melanogaster. Hemiclonal analysis estimates the additive genetic variation among random, genomewide haplotypes taken from a large, outbred, locally adapted laboratory population and determines the direction of the selection gradient on this variation. In contrast to earlier studies, we found low but biologically significant heritable variation for defensive and offensive offspring production as well as all their components (P1, fidelity, P2, and remating). Genetic correlations between these traits were substantially different from those reported for inbred lines. A positive genetic correlation was found between defense and offense, demonstrating that some shared genes influence both traits. In addition to this common variation, evidence for unique genetic variation for each trait was also found, supporting an ongoing coevolutionary arms race between defense and offense. Reproductive conflict between males can strongly influence female fitness. Correspondingly, we found genetic variation in both defense and offense that affected female fitness. No evidence was found for intersexual conflict in the context of male defense, but we found substantial intersexual conflict in the context of male offensive sperm competitive ability. These results indicate that conflict between competing males also promotes an associated arms race between the sexes.

Place, publisher, year, edition, pages
Lawrence, Kans.: Society for the Study of Evolution, 2005
Keyword
Coevolution, Drosophila melanogaster, interlocus intersexual conflict, interlocus intrasexual conflict, sexual selection, sperm competition
Identifiers
urn:nbn:se:umu:diva-5012 (URN)10.1111/j.0014-3820.2005.tb01803.x (DOI)16153039 (PubMedID)
Available from: 2006-03-30 Created: 2006-03-30 Last updated: 2011-03-25Bibliographically approved
4. Male perception of female mating status: its effect on copulation duration and male and female fitness in Drosophila melanogaster
Open this publication in new window or tab >>Male perception of female mating status: its effect on copulation duration and male and female fitness in Drosophila melanogaster
2006 (English)In: Animal Behaviour, ISSN 0003-3472, E-ISSN 1095-8282, Vol. 72, no 6, 1259-1268 p.Article in journal (Refereed) Published
Place, publisher, year, edition, pages
Elsevier, 2006
National Category
Biological Sciences
Identifiers
urn:nbn:se:umu:diva-5013 (URN)10.1016/j.anbehav.2006.03.021 (DOI)
Available from: 2006-03-30 Created: 2006-03-30 Last updated: 2012-06-14Bibliographically approved
5. Genetic variation in male and female reproductive characters associated with sexual conflict in Drosophila melanogaster
Open this publication in new window or tab >>Genetic variation in male and female reproductive characters associated with sexual conflict in Drosophila melanogaster
2005 (English)In: Behavior Genetics, ISSN 0001-8244, E-ISSN 1573-3297, Vol. 35, no 4, 455-462 p.Article in journal (Refereed) Published
Abstract [en]

Recent studies have shown that elevated mating, courtship and seminal substances affect female fitness negatively in Drosophila melanogaster. It has also been shown that males vary with respect to these characters and that male harm to females correlates positively with components of male fitness. These results suggest that there is sexual conflict over the effect of such male characters. An important component of this scenario is that females have evolved counteradaptations to male harm, but so far there is limited evidence for this. Here I define female resistance as the ability to withstand an increased exposure to males. Across 10 genetically differentiated lines of D. melanogaster, I found genetic variation among females in the reduction of lifespan that followed from exposure to males of different durations. There was also genetic variation among males with regards to the degree to which they decrease the lifespan of their mates. These results suggest that genetic variation for female ability to endure male sexually antagonistic adaptations exists and may play an important role in male–female coevolution.

Place, publisher, year, edition, pages
New York, N.Y.: Plenum Publishing Corp., 2005
Keyword
Drosophila melanogaster, female resistance, male harm, seminal fluid, sexual antagonism, sexual selection
Identifiers
urn:nbn:se:umu:diva-5014 (URN)10.1007/s10519-004-1246-8 (DOI)15971026 (PubMedID)
Available from: 2006-03-30 Created: 2006-03-30 Last updated: 2011-03-30Bibliographically approved
6. Inter-locus antagonistic coevolution as an engine of speciation: assessment with hemiclonal analysis
Open this publication in new window or tab >>Inter-locus antagonistic coevolution as an engine of speciation: assessment with hemiclonal analysis
Show others...
2005 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 102, no Suppl. 1, 6527-6534 p.Article in journal (Refereed) Published
Abstract [en]

One of Ernst Mayr's legacies is the consensus that the allopatry model is the predominant mode of speciation in most sexually reproducing lineages. In this model, reproductive isolation develops as a pleiotropic byproduct of the genetic divergence that develops among physically isolated populations. Presently, there is no consensus concerning which, if any, evolutionary process is primarily responsible for driving the specific genetic divergence that leads to reproductive isolation. Here, we focus on the hypothesis that inter-locus antagonistic coevolution drives rapid genetic divergence among allopatric populations and thereby acts as an important “engine” of speciation. We assert that only data from studies of experimental evolution, rather than descriptive patterns of molecular evolution, can provide definitive evidence for this hypothesis. We describe and use an experimental approach, called hemiclonal analysis, that can be used in theDrosophila melanogaster laboratory model system to simultaneously screen nearly the entire genome for both standing genetic variation within a population and the net-selection gradient acting on the variation. Hemiclonal analysis has four stages: (i) creation of a laboratory “island population”; (ii) cytogenetic cloning of nearly genome-wide haplotypes to construct hemiclones; (iii) measurement of additive genetic variation among hemiclones; and (iv) measurement of the selection gradient acting on phenotypic variation among hemiclones. We apply hemiclonal analysis to test the hypothesis that there is ongoing antagonistic coevolution between the sexes in the D. melanogaster laboratory model system and then discuss the relevance of this analysis to natural systems.

Place, publisher, year, edition, pages
Washington: National Academy of Sciences, 2005
Keyword
sexual conflict, inter-locus contest evolution, sexually antagonistic coevolution, reproductive isolation, genetic divergence
Identifiers
urn:nbn:se:umu:diva-5015 (URN)10.1073/pnas.0501889102 (DOI)
Available from: 2006-03-30 Created: 2006-03-30 Last updated: 2011-03-21Bibliographically approved
7. Sexual conflict promotes speciation in insects
Open this publication in new window or tab >>Sexual conflict promotes speciation in insects
2000 In: Proceedings of the National Academy of Sciences, ISSN 0027-8424, Vol. 97, no 19, 10460-10464 p.Article in journal (Refereed) Published
Identifiers
urn:nbn:se:umu:diva-5016 (URN)
Available from: 2006-03-30 Created: 2006-03-30Bibliographically approved

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