A meiotic driver alters sperm form and function in house mice: a possible example of spite

The ability to subvert independent assortment of chromosomes is found in many meiotic drivers, such as the t haplotype in house mice Mus musculus, in which the t-bearing chromosomal homolog is preferentially transmitted to offspring. This is explained by a poison-antidote system, in which developing + and t sperm in testes of + /t males are exposed to ‘poison’ coded by t loci, from which t sperm are protected, allowing t sperm an overwhelming fertilisation advantage in monogamous matings. This system is thought to result in poorly and normally motile sperm subpopulations within + /t sperm, leaving t sperm unharmed. Conversely, we found that the fastest quartile of sperm from + /t males swam more slowly, both forwards and along their travel path, and had reduced straightness and linearity, compared to the fastest quartile of + / + sperm. Moreover, sperm from + /t males had shorter tails and narrower heads than + / + sperm, and these morphological differences covaried with motility differences. Finally, + /t traits did not show evidence of bimodal distributions. We conclude that the t haplotype drive results in lasting damage to the motility of both + and t developing sperm, although previous studies indicate that + must be more harmed than t sperm. This damage to all sperm may explain the low success of + /t males in sperm competition with + / + males, seen in earlier studies. We propose that the harm the t causes to itself could be termed ‘spiteful’, which may also be common to other gamete-harming meiotic drive systems

Socially mediated polyandry: a new benefit of communal nesting in mammals

In many species, females have evolved behavioral strategies to reduce the risk of infanticide. For instance, polyandry can create paternity confusion that inhibits males from killing offspring they could have sired. Here, the authors propose that females could socially obtain the same benefits by nesting communally. Singly sired litters could be perceived as a large multiply sired litter once pooled together in a single nest. Long-term data from a wild house mouse population showed that monandrous litters (singly sired) were more common in communal than in solitary nests and 85% of them were raised with litters sired by different males hence becoming effectively polyandrous (multiply sired). These socially polyandrous litters had significantly higher offspring survival than genetically or socially monandrous litters and reached a similar survival to that of multiply sired litters raised in solitary or communal nests. Furthermore, the number of sires within nests significantly improved offspring survival whereas the number of mothers did not. These results suggest that the survival benefits associated with communal nesting are driven by polyandry and not communal defense. This socially mediated polyandry was as efficient as multiple paternity in preventing infanticide, and may also occur in other infanticidal and polytocous species where the caring parent exhibits social behavio

Direct selection on male attractiveness and female preference fails to produce a response

BACKGROUND: Theoretical studies suggest that direct and indirect selection have the potential to cause substantial evolutionary change in female mate choice. Similarly, sexual selection is considered a strong force in the evolution of male attractiveness and the exaggeration of secondary sexual traits. Few studies have, however, directly tested how female mate choice and male attractiveness respond to selection. Here we report the results of a selection experiment in which we selected directly on female mating preference for attractive males and, independently, on male attractiveness in the guppy, Poecilia reticulata. We measured the direct and correlated responses of female mate choice and male attractiveness to selection and the correlated responses of male ornamental traits, female fecundity and adult male and female survival. RESULTS: Surprisingly, neither female mate choice nor male attractiveness responded significantly to direct or to indirect selection. Fecundity did differ significantly among lines in a way that suggests a possible sexually-antagonistic cost to male attractiveness. CONCLUSIONS: The opportunity for evolutionary change in female mate choice and male attractiveness may be much smaller than predicted by current theory, and may thus have important consequences for how we understand the evolution of female mate choice and male attractiveness. We discuss a number of factors that may have constrained the response of female choice and male attractiveness to selection, including low heritabilities, low levels of genetic (co)variation in the multivariate direction of selection, sexually-antagonistic constraint on sexual selection and the "environmental covariance hypothesis"

The nasty neighbour in the striped mouse (Rhabdomys pumilio) steals paternity and elicits aggression

Background Territoriality functions to monopolize access to resources including mates, but is costly in terms of energy and time investment. Some species reduce these costs by being less aggressive towards their neighbours than towards unfamiliar strangers, the so called dear enemy phenomenon. However, in other species individuals are more, not less aggressive towards their neighbours. It has been hypothesised that this is due to the fact that neighbours can impose a greater threat than strangers, but this has not been tested previously. Results We tested aggression in wild group-living male striped mice in a neutral test arena and demonstrate that breeders are more aggressive than non-breeding philopatrics, and that more aggression occurs during the breeding than during the non-breeding season. Male breeders were significantly more aggressive towards their neighbours than towards strangers, leading to the prediction that neighbours are the most important competitors for paternity. Using a molecular parentage analysis we show that 28% of offspring are sired by neighbouring males and only 7% by strangers. Conclusions We conclude that in male striped mice the main function of male aggression is defending paternity against their territorial neighbours

Novel patterns of expression and recruitment of new genes on the t-haplotype, a mouse selfish chromosome

The t-haplotype of mice is a classical model for autosomal transmission distortion. A largely non-recombining variant of the proximal region of chromosome 17, it is transmitted to more than 90% of the progeny of heterozygous males through the disabling of sperm carrying a standard chromosome. While extensive genetic and functional work has shed light on individual genes involved in drive, much less is known about the evolution and function of the rest of its hundreds of genes. Here, we characterize the sequence and expression of dozens of t-specific transcripts and of their chromosome 17 homologues. Many genes showed reduced expression of the t-allele, but an equal number of genes showed increased expression of their t-copy, consistent with increased activity or a newly evolved function. Genes on the t-haplotype had a significantly higher non-synonymous substitution rate than their homologues on the standard chromosome, with several genes harbouring dN/dS ratios above 1. Finally, the t-haplotype has acquired at least two genes from other chromosomes, which show high and tissue-specific expression. These results provide a first overview of the gene content of this selfish element, and support a more dynamic evolutionary scenario than expected of a large genomic region with almost no recombination

Poecilia picta, a Close Relative to the Guppy, Exhibits Red Male Coloration Polymorphism: A System for Phylogenetic Comparisons

Studies on the evolution of female preference and male color polymorphism frequently focus on single species since traits and preferences are thought to co-evolve. The guppy, Poecilia reticulata, has long been a premier model for such studies because female preferences and orange coloration are well known to covary, especially in upstream/downstream pairs of populations. However, focused single species studies lack the explanatory power of the comparative method, which requires detailed knowledge of multiple species with known evolutionary relationships. Here we describe a red color polymorphism in Poecilia picta, a close relative to guppies. We show that this polymorphism is restricted to males and is maintained in natural populations of mainland South America. Using tests of female preference we show female P. picta are not more attracted to red males, despite preferences for red/orange in closely related species, such as P. reticulata and P. parae. Male color patterns in these closely related species are different from P. picta in that they occur in discrete patches and are frequently Y chromosome-linked. P. reticulata have an almost infinite number of male patterns, while P. parae males occur in discrete morphs. We show the red male polymorphism in P. picta extends continuously throughout the body and is not a Y-linked trait despite the theoretical prediction that sexually-selected characters should often be linked to the heterogametic sex chromosome. The presence/absence of red male coloration of P. picta described here makes this an ideal system for phylogenetic comparisons that could reveal the evolutionary forces maintaining mate choice and color polymorphisms in this speciose group

Novel patterns of expression and recruitment of new genes on the t-haplotype, a mouse selfish chromosome

The t-haplotype of mice is a classical model for autosomal transmission distortion. A largely non-recombining variant of the proximal region of chromosome 17, it is transmitted to more than 90% of the progeny of heterozygous males through the disabling of sperm carrying a standard chromosome. While extensive genetic and functional work has shed light on individual genes involved in drive, much less is known about the evolution and function of the rest of its hundreds of genes. Here, we characterize the sequence and expression of dozens of t-specific transcripts and of their chromosome 17 homologues. Many genes showed reduced expression of the t-allele, but an equal number of genes showed increased expression of their t-copy, consistent with increased activity or a newly evolved function. Genes on the t-haplotype had a significantly higher non-synonymous substitution rate than their homologues on the standard chromosome, with several genes harbouring dN/dS ratios above 1. Finally, the t-haplotype has acquired at least two genes from other chromosomes, which show high and tissue-specific expression. These results provide a first overview of the gene content of this selfish element, and support a more dynamic evolutionary scenario than expected of a large genomic region with almost no recombination

Parent‐offspring inference in inbred populations

Genealogical relationships are fundamental components of genetic studies. However, it is often challenging to infer correct and complete pedigrees even when genome-wide information is available. For example, inbreeding can obscure genetic differences between individuals, making it difficult to even distinguish first-degree relatives such as parent-offspring from full siblings. Similarly, genotyping errors can interfere with the detection of genetic similarity between parents and their offspring. Inbreeding is common in natural, domesticated, and experimental populations and genotyping of these populations often has more errors than in human data sets, so efficient methods for building pedigrees under these conditions are necessary. Here, we present a new method for parent-offspring inference in inbred pedigrees called specific parent-offspring relationship estimation (spore). spore is vastly superior to existing pedigree-inference methods at detecting parent-offspring relationships, in particular when inbreeding is high or in the presence of genotyping errors, or both. spore therefore fills an important void in the arsenal of pedigree inference tools

Polyandry and the Decrease of a Selfish Genetic Element in a Wild House Mouse Population

Despite deleterious effects on individuals, the t haplotype is a selfish genetic element present in many house mouse populations. By distorting the transmission ratio, +/t males transmit the t haplotype to up to 90% of their offspring. However, t/t individuals perish in utero. Theoretical models based on these properties predict a much higher t frequency than observed, leading to the t paradox. Here, we use empirical field data and theoretical approaches to investigate whether polyandry is a female counterstrategy against the negative fitness consequences of such distorters. We found a significant decrease of the t frequency over a period of 5.5 years that cannot be explained by the effect of transmission ratio distortion and recessive lethals, despite significantly higher life expectancy of +/t females compared to +/+ females. We quantified life-history data and homozygous and heterozygous fitness effects. Population subdivision and inbreeding were excluded as evolutionary forces influencing the t system. The possible influence of polyandry on the t system was then investigated by applying a stochastic model to this situation. Simulations show that polyandry can explain the observed t dynamics, making it a biologically plausible explanation for low t frequencies in natural populations in general

Cooperation by necessity: condition- and density-dependent reproductive tactics of female house mice

Optimal reproductive strategies evolve from the interplay between an individual’s intrinsic state and extrinsic environment, both factors that are rarely fixed over its lifetime. Conditional breeding tactics might be one evolutionary trajectory allowing individuals to maximize fitness. We apply multi-state capture-mark-recapture analysis to a detailed 8-year data set of free-ranging house mice in a growing population to discern causes and fitness consequences of two alternative reproductive tactics in females, communal and solitary breeding. This allows us to integrate natural variation in life-history traits when analysing the expression of two alternative reproductive tactics in females. We find that communal breeding reduces average population fitness, but nevertheless increases over our 8-year study period. The tactic proves to be expressed conditionally dependent on both population density and female body mass – allowing females to breed under subpar conditions, i.e. at high density or when of low body mass. Our results contradict previous laboratory studies and emphasize the importance of studying cooperation under natural conditions, including natural variation in state-dependent survival and breeding probabilities