Tom A. R. Price

The Ecology and Evolutionary Dynamics of Meiotic Drive

Meiotic drivers are genetic variants that selfishly manipulate the production of gametes to increase their own rate of transmission, often to the detriment of the rest of the genome and the individual that carries them. This genomic conflict potentially occurs whenever a diploid organism produces a haploid stage, and can have profound evolutionary impacts on gametogenesis, fertility, individual behaviour, mating system, population survival, and reproductive isolation. Multiple research teams are developing artificial drive systems for pest control, utilising the transmission advantage of drive to alter or exterminate target species. Here, we review current knowledge of how natural drive systems function, how drivers spread through natural populations, and the factors that limit their invasion.

Selfish genetic elements and sexual selection: their impact on male fertility.

Females of many species mate with more than one male (polyandry), yet the adaptive significance of polyandry is poorly understood. One hypothesis to explain the widespread occurrence of multiple mating is that it may allow females to utilize post-copulatory mechanisms to reduce the risk of fertilizing their eggs with sperm from incompatible males. Selfish genetic elements (SGEs) are ubiquitous in eukaryotes, frequent sources of reproductive incompatibilities, and associated with fitness costs. However, their impact on sexual selection is largely unexplored. In this review we examine the link between SGEs, male fertility and sperm competitive ability. We show there is widespread evidence that SGEs are associated with reduced fertility in both animals and plants, and present some recent data showing that males carrying SGEs have reduced paternity in sperm competition. We also discuss possible reasons why male gametes are particularly vulnerable to the selfish actions of SGEs. The widespread reduction in male fertility caused by SGEs implies polyandry may be a successful female strategy to bias paternity against SGE-carrying males.

Sex ratio distorter reduces sperm competitive ability in an insect.

Abstract Selfish genetic elements (SGEs) are ubiquitous in animals and often associated with low male fertility due to reduced sperm number in male carriers. In the fruit fly Drosophila pseudoobscura, the meiotic driving X chromosome “sex ratio” kills Y-bearing sperm in carrier males (SR males), resulting in female only broods. We competed SR males against the ejaculates of noncarrying standard males (ST males), and quantified the number of sperm transferred by SR and ST males to females. We show that SR males are very poor sperm competitors, which is partly related to transfer of fewer sperm during mating. However, sperm numbers alone cannot explain the observed paternity reduction, indicating SR males’ sperm may be of reduced quality, possibly due to damage during the killing of the noncarrying Y-sperm. The reduction in sperm competitive ability due to SR is large enough to potentially stabilize the spread of sex ratio drive through populations. The poor sperm competitive ability of SR males coupled with their low fitness as mates could favor increased remating by females to reduce paternity by SR males. Given the generally poor performance of SGE-carrying males in sperm competition, this may generate strong selective pressure favoring polyandry in many species.

Age-based female preference in the fruit fly Drosophila pseudoobscura

With respect to mate choice, females of many species discriminate between males on the basis of age. The adaptive significance of age-based mate choice is unclear, with various hypotheses making conflicting predictions. We examined the possibility of female preference in the fruit fly Drosophila pseudoobscura, a species where females gain no significant nutritional benefits from mating. Females were shown to prefer to mate with old males in two-male choice experiments and accepted old males faster than young males in single-male tests. Females mated to old males had a higher fecundity, possibly related to a transfer of more sperm and/or a larger volume of accessory gland proteins during the longer copulation durations experienced with old males, although these possibilities were not directly tested. Hence, females appear to derive direct benefits from preferring to mate with older males. In contrast, there was no evidence of mate preference for the sons of either old or young males when matched for age, indicating that the mating advantage of old males is not passed to their sons. These sets of experiments suggest that in D. pseudoobscura the benefit of age-based preference to females is increased fecundity due to greater investment per mating by older males.

Experience of mating rivals causes males to modulate sperm transfer in the fly Drosophila pseudoobscura.

Male responses to risk of sperm competition play an important role in sexual selection, sexual conflict, and the evolution of mating systems. Such responses can combine behavioural and physiological processes, and can be mediated through different components of the ejaculate such as sperm numbers and seminal proteins. An additional level of ejaculate complexity is sperm heteromorphism, with the inclusion of non-fertilising parasperm in the ejaculate. We now test the response to rivals in a sperm heteromorphic species, Drosophila pseudoobscura, measuring the behavioural response and sperm transfer and, crucially, relating these to short-term fitness. Males respond to exposure to conspecific rivals by increasing mating duration, but do not respond to heterospecific rivals. In addition, after exposure to a conspecific rival, males increased the transfer of fertilising eusperm, but not non-fertilising parasperm. Males exposed to a conspecific rival also achieve higher offspring production. This suggests that the evolution of parasperm in flies was not driven by sperm competition and adds to the increasing evidence that males can make extremely sophisticated responses to mating competition.

Remating in the laboratory reflects rates of polyandry in the wild

Much of our understanding of female mating behaviour in insects comes from studies performed under controlled laboratory conditions, with Drosophila as the most commonly used model system. Laboratory studies of Drosophila have demonstrated a strong genetic basis to female remating rate. Because behaviour is strongly influenced by the environment, the heritability of remating rate in laboratory cultures does not necessarily reflect variation that is relevant to field conditions. In this study, we investigated the strength of the link between the behaviour of flies in laboratory and field. Wild-caught female Drosophila pseudoobscura that produced broods sired by multiple males had daughters that remated more rapidly in the laboratory. This suggests that laboratory experiments can successfully reflect differences between females’ mating behaviour in nature.

Does polyandry control population sex ratio via regulation of a selfish gene

The extent of female multiple mating (polyandry) can strongly impact on the intensity of sexual selection, sexual conflict, and the evolution of cooperation and sociality. More subtly, polyandry may protect populations against intragenomic conflicts that result from the invasion of deleterious selfish genetic elements (SGEs). SGEs commonly impair sperm production, and so are likely to be unsuccessful in sperm competition, potentially reducing their transmission in polyandrous populations. Here, we test this prediction in nature. We demonstrate a heritable latitudinal cline in the degree of polyandry in the fruitfly Drosophila pseudoobscura across the USA, with northern population females remating more frequently in both the field and the laboratory. High remating was associated with low frequency of a sex-ratio-distorting meiotic driver in natural populations. In the laboratory, polyandry directly controls the frequency of the driver by undermining its transmission. Hence we suggest that the cline in polyandry represents an important contributor to the cline in sex ratio in nature. Furthermore, as the meiotic driver causes sex ratio bias, variation in polyandry may ultimately determine population sex ratio across the USA, a dramatic impact of female mating decisions. As SGEs are ubiquitous it is likely that the reduction of intragenomic conflict by polyandry is widespread.

DDT resistance, epistasis and male fitness in flies

In Drosophila melanogaster, the DDT resistance allele (DDT‐R) is beneficial in the presence of DDT. Interestingly, DDT‐R also elevates female fitness in the absence of DDT and existed in populations before DDT use. However, DDT‐R did not spread regardless of DDT‐independent selective advantages in females. We ask whether sexual antagonism could explain why DDT‐R did not spread before pesticide use. We tested pre‐ and post‐copulatory male fitness correlates in two genetic backgrounds into which we backcrossed the DDT‐R allele. We found costs to DDT‐R that depended on the genetic background in which DDT‐R was found and documented strong epistasis between genetic background and DDT‐R that influenced male size. Although it remains unclear whether DDT‐R is generally sexually antagonistic, or whether the fitness costs noted would be sufficient to retard the spread of DDT‐R in the absence of DDT, general fitness advantages to DDT‐R in the absence of DDT may be unlikely.

True polyandry and pseudopolyandry: why does a monandrous fly remate?

BackgroundThe rate of female remating can have important impacts on a species, from affecting conflict and cooperation within families, to population viability and gene flow. However, determining the level of polyandry in a species can be difficult, with information on the mating system of many species being based on a single experiment, or completely absent. Here we investigate the mating system of the fruit fly Drosophila subobscura. Reports from England, Spain and Canada suggest D. subobscura is entirely monandrous, with no females remating. However, work in Greece suggests that 23% of females remate. We examine the willingness of female D. subobscura to remate in the laboratory in a range of conditions, using flies from both Greece and England. We make a distinction between pseudopolyandry, where a female remates after an ineffective first mating that is incapable of fertilising her eggs, and true polyandry, where a female remates even though she has received suitable sperm from a previous mating.ResultsWe find a low rate of true polyandry by females (4%), with no difference between populations. The rate of true polyandry is affected by temperature, but not starvation. Pseudopolyandry is three times as common as true polyandry, and most females showing pseudopolyandry mated at their first opportunity after their first failed mating. However, despite the lack of differences in polyandry between the populations, we do find differences in the way males respond to exposure to other males prior to mating. In line with previous work, English flies responded to one or more rivals by increasing their copulation duration, a response previously thought to be driven by sperm competition. Greek males only show increased copulation duration when exposed to four or more rival males. This suggests that the response to rivals in D. subobscura is not related to sperm competition, because sperm competition is rare, and there is no correlation of response to rivals and mating system across the populations.ConclusionsThese results illustrate the difficulties in determining the mating system of a species, even one that is well known and an excellent laboratory species, with results being highly dependent on the conditions used to assay the behaviour, and the population used.

No evidence of mate discrimination against males carrying a sex ratio distorter in Drosophila pseudoobscura

Selfish genetic elements (SGEs) that spread by manipulating spermatogenesis often have highly deleterious effects on males that carry them. Females that mate with male carriers of SGEs can also suffer significant costs: they receive fewer and poorer-quality sperm, their offspring will inherit the deleterious allele, and the sex ratio of their offspring will be biased towards the more common sex. To counter these costs, females are therefore expected to prefer to mate with males that do not carry sex ratio distorters or other deleterious selfish genetic elements. However, despite the potential costs, there are few examples of female choice against males carrying SGEs. We searched for evidence of a female preference in fruit fly Drosophila pseudoobscura against males carrying a costly meiotic driving X-chromosome Sex Ratio (SR). In a series of five non-competitive mate preference experiments, we find no evidence that females prefer to mate with non-SR males. Our use of five separate experiments, involving more than 800 females, makes it unlikely that this lack of a difference was due to low power or simple chance. We suggest that the lack of female choice against SGE-carrying males may be due to strong selection on SGEs to be indistinguishable from alternative alleles. Furthermore, polyandry, either in direct response to receiving an ejaculate from an SGE-carrying male or carried out indiscriminately when at risk of mating with carriers, may be an alternative response by females to limit the exposure of their offspring to SGEs.