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Sexual Selection in House Mice (Mus musculus domesticus) and the Role of a Selfish Genetic Element


Sutter, Andreas. Sexual Selection in House Mice (Mus musculus domesticus) and the Role of a Selfish Genetic Element. 2016, University of Zurich, Faculty of Science.

Abstract

According to the Mendelian rules of inheritance, every chromosome or allele of a diploid organism has a 50% chance of being transmitted to a given offspring. These rules are violated by selfish genetic elements which distort transmission to increase their own representation in the next generation. This contrasts with the traditional Darwinian view of evolution, under which genetic variants that confer a fitness benefit to their bearers should propagate. Indeed, selfish genetic elements can increase in frequency even if they decrease the fitness of the whole organism, which causes intra-genomic conflict between the selfish genetic element and the rest of the genome. The genome as a whole will thus attempt to suppress the costly actions of selfish genetic elements. This thesis explores how the behaviour of the organism might act as a suppressor of intra-genomic conflict in house mice.
The t haplotype is a well-known example of a selfish genetic element that is found in house mice. It is a large stretch of DNA that manipulates male gametogenesis to subvert Mendelian inheritance (i.e., it shows ‘meiotic drive’). Moreover, the t haplotype carries recessive embryonic lethal mutations that impose a strong fitness cost on the rest of the genome. Its selfishness at the gamete level allows it to persist despite its negative effect of the fitness of its bearers. Given that females invest heavily into offspring, and that the t haplotype has severe negative effects on offspring viability, females should avoid fertilisation by males carrying the t haplotype (+/t males). Because the male drive mechanism affects sperm, postcopulatory sexual selection offers a particularly promising mechanism for avoiding fertilisation by +/t males. The first three chapters of this thesis investigate the effects of pre- and postcopulatory sexual selection on the t haplotype, and how the t haplotype may in turn affect sexual selection in house mice. Chapters 4 and 5 extend the investigation of male reproductive strategies in sperm competition.
CHAPTER 1 addresses how the t haplotype’s manipulation of spermatogenesis affects the sperm competitiveness of +/t males. When a female mates with multiple males during a single reproductive episode, the sperm from different males can overlap and compete over fertilisation of the female’s ova. The relative number and speed of a male’s sperm determine his fertilisation likelihood. Because the t haplotype sabotages half of a +/t male’s sperm, this should reduce the competitiveness of a +/t ejaculate against a wild type male’s ejaculate. Moreover, the intra-ejaculate sabotage might come at an additional cost to the t bearing sperm. Females may benefit from this if mating with multiple males reduces the success of +/t males, which increases offspring viability and quality. The outcome of controlled sperm competition trials between +/t and +/+ males showed that +/t males are indeed severely disadvantaged against +/+ males, and that the strength of the effect is stronger than expected if the drive mechanism left t bearing sperm unaffected. As a consequence, multiply mated +/t females have more viable embryos than females mated only to a +/t male. Polyandry thus offers a mechanism for avoiding costly fertilisation by costly +/t males.
CHAPTER 2 expands the investigation of the effects of the +/t haplotype on sperm competition to investigate how reduced sperm competitiveness may have repercussions on male reproductive strategies. When wild type males mate with a previously unmated female, they sire the majority of her offspring, regardless of whether the female successively mates with an additional male. A +/t male on the other hand loses more if a female he has mated with remates with another male, given the low sperm competitiveness of +/t males. We may thus expect +/t males to invest more into mate guarding to secure paternity. Interestingly, sperm competition between two +/t males showed that +/t males are generally disadvantaged in the first-to-mate role, which is in strong contrast with the general paternity advantage of wild type (+/+) males when first-to-mate. This accentuates the difference in the incentive for mate guarding between +/t and +/+ males. However, none of the hypothesised differences in reproductive strategies were found between +/t and +/+ males, suggesting that mate guarding might not be a feasible strategy for male house mice, or that the t haplotype is unable to exert control over polygenic behavioural traits.
In CHAPTER 3, active female discrimination against +/t males is investigated at different stages before and after mating. Previous research showed that females preferred the smell of +/+ males over that of +/t males, but a recent experiment that looked at an actual mating context found no evidence for precopulatory female discrimination against +/t males. The results reported in this thesis showed that females were not more likely to mate with +/+ males than with +/t males. Moreover, females did not accept ejaculation by +/+ males more quickly, were not more likely to remate after mating with a +/t male and did not show any evidence for preferential fertilisation by wild type sperm over t bearing sperm from within a +/t male’s ejaculate. These findings indicate that females may not be able to detect male t genotype and to physiologically counteract male drive at the gamete level. Alternatively, females may simply rely on polyandry as an effective strategy against drive-mediated fitness costs.
Sperm competition favours male adaptations that increase competitive fertilisation success or decrease female multiple mating. Males of many species produce copulatory plugs that obstruct the female’s genitals after ejaculation, which has generally been interpreted as a male adaptation to sperm competition. However, copulatory plugs might have other functions, and empirical tests of a function of the copulatory plug in sperm competition have provided mixed results over a variety of animal taxa. The results of CHAPTER 4 showed that male mice are strongly limited in the ejaculate components that the copulatory plug is made of, as evidenced by a reduction in plug size concomitant with repeated ejaculation. Males that produce smaller plugs appear to delay the ejaculation of rival males less, and possibly as a consequence, father fewer offspring. In CHAPTER 5, copulatory plugs were experimentally removed, and the consequences for copulatory behaviour and paternity were analysed in more detail. The results confirmed that large copulatory plugs delay rival male ejaculation, with positive consequences for the paternity success of first-to-mate males.
The research presented in this thesis demonstrates the strong impact of sexual selection—particularly of postcopulatory sexual selection—on the t haplotype, and highlights potential consequences for wild house mouse populations. Sexual behaviour at the organismal level that exposes the downside of the actions of male drive offers a way to suppress conflict at the gene level. This thesis also advances our understanding of mechanistic aspects of sperm competition and of the relationship between sperm features and fertilisation in a vertebrate model species.

According to the Mendelian rules of inheritance, every chromosome or allele of a diploid organism has a 50% chance of being transmitted to a given offspring. These rules are violated by selfish genetic elements which distort transmission to increase their own representation in the next generation. This contrasts with the traditional Darwinian view of evolution, under which genetic variants that confer a fitness benefit to their bearers should propagate. Indeed, selfish genetic elements can increase in frequency even if they decrease the fitness of the whole organism, which causes intra-genomic conflict between the selfish genetic element and the rest of the genome. The genome as a whole will thus attempt to suppress the costly actions of selfish genetic elements. This thesis explores how the behaviour of the organism might act as a suppressor of intra-genomic conflict in house mice.
The t haplotype is a well-known example of a selfish genetic element that is found in house mice. It is a large stretch of DNA that manipulates male gametogenesis to subvert Mendelian inheritance (i.e., it shows ‘meiotic drive’). Moreover, the t haplotype carries recessive embryonic lethal mutations that impose a strong fitness cost on the rest of the genome. Its selfishness at the gamete level allows it to persist despite its negative effect of the fitness of its bearers. Given that females invest heavily into offspring, and that the t haplotype has severe negative effects on offspring viability, females should avoid fertilisation by males carrying the t haplotype (+/t males). Because the male drive mechanism affects sperm, postcopulatory sexual selection offers a particularly promising mechanism for avoiding fertilisation by +/t males. The first three chapters of this thesis investigate the effects of pre- and postcopulatory sexual selection on the t haplotype, and how the t haplotype may in turn affect sexual selection in house mice. Chapters 4 and 5 extend the investigation of male reproductive strategies in sperm competition.
CHAPTER 1 addresses how the t haplotype’s manipulation of spermatogenesis affects the sperm competitiveness of +/t males. When a female mates with multiple males during a single reproductive episode, the sperm from different males can overlap and compete over fertilisation of the female’s ova. The relative number and speed of a male’s sperm determine his fertilisation likelihood. Because the t haplotype sabotages half of a +/t male’s sperm, this should reduce the competitiveness of a +/t ejaculate against a wild type male’s ejaculate. Moreover, the intra-ejaculate sabotage might come at an additional cost to the t bearing sperm. Females may benefit from this if mating with multiple males reduces the success of +/t males, which increases offspring viability and quality. The outcome of controlled sperm competition trials between +/t and +/+ males showed that +/t males are indeed severely disadvantaged against +/+ males, and that the strength of the effect is stronger than expected if the drive mechanism left t bearing sperm unaffected. As a consequence, multiply mated +/t females have more viable embryos than females mated only to a +/t male. Polyandry thus offers a mechanism for avoiding costly fertilisation by costly +/t males.
CHAPTER 2 expands the investigation of the effects of the +/t haplotype on sperm competition to investigate how reduced sperm competitiveness may have repercussions on male reproductive strategies. When wild type males mate with a previously unmated female, they sire the majority of her offspring, regardless of whether the female successively mates with an additional male. A +/t male on the other hand loses more if a female he has mated with remates with another male, given the low sperm competitiveness of +/t males. We may thus expect +/t males to invest more into mate guarding to secure paternity. Interestingly, sperm competition between two +/t males showed that +/t males are generally disadvantaged in the first-to-mate role, which is in strong contrast with the general paternity advantage of wild type (+/+) males when first-to-mate. This accentuates the difference in the incentive for mate guarding between +/t and +/+ males. However, none of the hypothesised differences in reproductive strategies were found between +/t and +/+ males, suggesting that mate guarding might not be a feasible strategy for male house mice, or that the t haplotype is unable to exert control over polygenic behavioural traits.
In CHAPTER 3, active female discrimination against +/t males is investigated at different stages before and after mating. Previous research showed that females preferred the smell of +/+ males over that of +/t males, but a recent experiment that looked at an actual mating context found no evidence for precopulatory female discrimination against +/t males. The results reported in this thesis showed that females were not more likely to mate with +/+ males than with +/t males. Moreover, females did not accept ejaculation by +/+ males more quickly, were not more likely to remate after mating with a +/t male and did not show any evidence for preferential fertilisation by wild type sperm over t bearing sperm from within a +/t male’s ejaculate. These findings indicate that females may not be able to detect male t genotype and to physiologically counteract male drive at the gamete level. Alternatively, females may simply rely on polyandry as an effective strategy against drive-mediated fitness costs.
Sperm competition favours male adaptations that increase competitive fertilisation success or decrease female multiple mating. Males of many species produce copulatory plugs that obstruct the female’s genitals after ejaculation, which has generally been interpreted as a male adaptation to sperm competition. However, copulatory plugs might have other functions, and empirical tests of a function of the copulatory plug in sperm competition have provided mixed results over a variety of animal taxa. The results of CHAPTER 4 showed that male mice are strongly limited in the ejaculate components that the copulatory plug is made of, as evidenced by a reduction in plug size concomitant with repeated ejaculation. Males that produce smaller plugs appear to delay the ejaculation of rival males less, and possibly as a consequence, father fewer offspring. In CHAPTER 5, copulatory plugs were experimentally removed, and the consequences for copulatory behaviour and paternity were analysed in more detail. The results confirmed that large copulatory plugs delay rival male ejaculation, with positive consequences for the paternity success of first-to-mate males.
The research presented in this thesis demonstrates the strong impact of sexual selection—particularly of postcopulatory sexual selection—on the t haplotype, and highlights potential consequences for wild house mouse populations. Sexual behaviour at the organismal level that exposes the downside of the actions of male drive offers a way to suppress conflict at the gene level. This thesis also advances our understanding of mechanistic aspects of sperm competition and of the relationship between sperm features and fertilisation in a vertebrate model species.

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Additional indexing

Item Type:Dissertation
Referees:Lindholm Anna K, König Barbara, Blanckenhorn Wolf U
Communities & Collections:07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
Dewey Decimal Classification:570 Life sciences; biology
590 Animals (Zoology)
Uncontrolled Keywords:sperm competition, sexual selection, intragenomic conflict, meiotic drive, t haplotype, house mouse
Language:English
Date:2016
Deposited On:19 Sep 2016 10:42
Last Modified:19 Sep 2016 10:42
Number of Pages:138
Funders:Swiss National Science Foundation
Permanent URL: https://doi.org/10.5167/uzh-126106

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