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Box plot (Q1, median, Q3) of ms395 allele sizes found at 12 sites along the Gombak valley (see for locations). Whiskers (Q1−1.5*interquartile range (IQR), Q3+1.5*IQR) show the spread of the allele sizes and outliers (mainly large alleles). Six of the 12 sites (circled) show the presence of large ms395 alleles (>218 bp), whereas the other six sites show a complete absence of large alleles.
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This study provides the first direct evidence from wild populations of stalk-eyed flies to support the hypothesis that male eyespan is a signal of meiotic drive. Several stalk-eyed fly species are known to exhibit X-linked meiotic drive. A recent quantitative trait locus analysis in Teleopsis dalmanni found a potential link between variation in mal...
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Male and female genital morphology varies widely across many taxa, and even among populations. Disentangling potential sources of selection on genital morphology is problematic because each sex is predicted to respond to adaptations in the other due to reproductive conflicts of interest. To test how variation in this sexual conflict trait relates t...
Citations
... Females have evolved responses or preferences to prevent them from mating with SGE carriers in some cases. In stalk-eyed flies, females preferentially mate with males with wider eye spans, whereas SGE-carrying males are generally associated with smaller eye spans (Cotton et al., 2014;Wilkinson et al., 1988). The presence of sperm-killing meiotic drive also correlates with the rate of polyandry in populations, where meiotic drive is more common in areas with low polyandry (Pinzone & Dyer, 2013;Price et al., 2014). ...
... The stalk-eyed fly XCMD SR chromosome is linked to males having smaller eye spans and reduced attractiveness (Cotton et al., 2014;Wilkinson et al., 1988). Such a system allows females to avoid mating with SR males, thus also avoiding the costs that SR imposes (Finnegan et al., 2019). ...
X chromosome meiotic drive (XCMD) kills Y‐bearing sperm during spermatogenesis, leading to the biased transmission of the selfish X chromosome. Despite this strong transmission, some natural XCMD systems remain at low and stable frequencies, rather than rapidly spreading through populations. The reason may be that male carriers can have reduced fitness, as they lose half of their sperm, only produce daughters, and may carry deleterious alleles associated with XCMD. Thus, females may benefit from avoiding mating with male carriers, yielding a further reduction in fitness. Genetic suppressors of XCMD, which block the killing of Y sperm and restore fair Mendelian inheritance, are also common and could prevent the spread of XCMD. However, whether suppressed males are as fit as a wild‐type male remains an open question, as the effect that genetic suppressors may have on a male's mating success is rarely considered. Here, we investigate the mating ability of XCMD males and suppressed XCMD males in comparison to wild‐type males in the fruit fly Drosophila subobscura, where drive remains at a stable frequency of 20% in wild populations where it occurs. We use both competitive and non‐competitive mating trials to evaluate male mating success in this system. We found no evidence that unsuppressed XCMD males were discriminated against. Remarkably, however, their suppressed XCMD counterparts had a higher male mating success compared to wild‐type controls. Unsuppressed XCMD males suffered 12% lower offspring production in comparison to wild‐type males. This cost appears too weak to counter the transmission advantage of XCMD, and thus the factors preventing the spread of XCMD remain unclear.
... In summary, we demonstrate that meiotic drive is not always associated with male fertility reduction under conditions of sperm competition, even though drive destroys half of carrier-male sperm. The lack of a fertility cost potentially contributes to the relatively high frequency of meiotic drive in T. dalmanni, which is around 20% in wild populations (Cotton et al., 2014;Paczolt et al., 2017;Wilkinson et al., 2003). This pattern is unlike other species where drive males do poorly under sperm competition and the spread of drive is reliant on a high frequency of monandrous matings (Courret et al., 2019;Dyer and Hall, 2019;Price et al., 2008b). ...
Male X-linked meiotic drive systems, which cause the degeneration of Y-bearing sperm, are common in the Diptera. Sperm killing is typically associated with fitness costs that arise from the destruction of wildtype sperm and collateral damage to maturing drive sperm, resulting in poor success under sperm competition. We investigate X-linked meiotic drive fertility in the stalk-eyed fly, Teleopsis dalmanni. Drive male paternity was measured in double mating trials under sperm competition against a wildtype male. Drive males sired the same number of offspring as wildtype males, both when mated first or second. This is the first evidence that drive males can compete equally with non-drive males in double matings, challenging the assumption that drive males inevitably suffer reduced fertility. The finding is in accord with previous work showing that the number of sperm per ejaculate transferred to females during non-competitive single matings does not differ between drive and wildtype males, which is likely due to the adaptive evolution of enlarged testes in drive males. Future experiments will determine whether the competitive ability of drive males is maintained under higher rates of female remating likely to be experienced in nature.
... Eyestalk length is an allometric, condition-dependent ornament [19,20], where males bearing long eyestalks experience an advantage in both female choice and male-male competition [21][22][23]. SR males have shorter eyestalks relative to body size when compared to ST males [13,24] and should thus be at a disadvantage in pre-copulatory sexual selection, which is expected to contribute to maintenance of the drive polymorphism [6]. Several lines of evidence [25,26] indicate that post-copulatory sexual selection is also important in this species. ...
... As expected, the frequency of the X SR chromosome and the eclosion sex ratio rapidly increased in the paired treatment lines, some of which would have gone extinct if we had not imposed a limit on the breeding sex ratio. Interestingly, the serial and group treatments controlled X SR frequency to a similar extent despite the known genetic association between X chromosome type and male eyespan [13,24]. These results are consistent with a previous experimental evolution study which removed sexual selection and found that multiple mating in female D. pseudoobscura was sufficient to limit the sex ratio phenotype and prevent line extinction [43,44]. ...
... Experimental evolution also reveals that selection can affect male eyespan, a sexually selected allometric trait, in multiple ways. Given that the X SR chromosome is known to have a strong effect on male eyespan [13,24], we compared relative eyespan by chromosome type in each mating treatment to avoid confounding eyespan change due solely to change in X SR frequency. We expected that reduced intensity of pre-copulatory sexual selection imposed by the paired and serial treatments would result in reduced male eyespan compared to the group treatment; however, we did not observe that outcome. ...
This paper describes the results of an experimental evolution study in which sexual selection was manipulated by controlling female mating opportunities and the presence of a distorting X chromosome in the stalk-eyed fly, Teleopsis dalmanni,
over 11 generations. Removal of sexual selection leads to an
increase in the frequency of the X-linked distorter and sex ratio across generations, but post-copulatory sexual selection alone is sufficient to limit the
frequency of distorters. In addition, male eyestalk length, a trait
under pre-copulatory sexual selection, evolves in response to changes in the
strength of sexual selection with the magnitude of the response dependent
on X chromosome type and the frequency of distorting X chromosomes.
These results reveal how a selfish X can interact with sexual selection to
influence the evolution of sexually selected traits in multiple ways.
... In this species, 10-30% of males possess X-linked elements that prevent proper development of Y-bearing sperm and result in carrier males producing 90% or more daughters (Presgraves et al. 1997). This SR X chromosome has multiple impacts on individual fitness (Wilkinson et al. 2006;Finnegan et al. 2019;Meade et al. 2019) including reduced sexual ornament (eyespan) size in SR males (Wilkinson et al. 1998;Johns et al. 2005;Cotton et al. 2014). The SR X chromosome (X SR ) appears to have originated approximately 500 Kya (Paczolt et al. 2017), and hundreds of mostly X-linked genes are differentially expressed in the testes of SR males (Reinhardt et al. 2014). ...
Stalk-eyed flies in the genus Teleopsis carry selfish genetic elements that induce sex ratio meiotic drive (SR) and impact the fitness of male and female carriers. Here, we assemble and describe a chromosome-level genome assembly of the stalk-eyed fly, Teleopsis dalmanni, to elucidate patterns of divergence associated with SR. The genome contains tens of thousands of transposable element (TE) insertions and hundreds of transcriptionally and insertionally active TE families. By resequencing pools of SR and ST males using short and long-reads, we find widespread differentiation and divergence between XSR and XST associated with multiple nested inversions involving most of the sex ratio haplotype. Examination of genomic coverage and gene expression data revealed seven X-linked genes with elevated expression and coverage in SR males. The most extreme and likely drive candidate involves an XSR-specific expansion of an array of partial copies of JASPer, a gene necessary for maintenance of euchromatin and associated with regulation of TE expression. In addition, we find evidence for rapid protein evolution between XSR and XST for testis expressed and novel genes, i.e. either recent duplicates or lacking a dipteran ortholog, including an X-linked duplicate of maelstrom, which is also involved in TE silencing. Overall, the evidence suggests that this ancient XSR polymorphism has had a variety of impacts on repetitive DNA and its regulation in this species.
... In summary, we demonstrate that meiotic drive is not always associated with male fertility reduction under conditions of sperm competition, even though drive destroys half of carrier-male sperm. The lack of a fertility cost potentially contributes to the relatively high frequency of meiotic drive in T. dalmanni, which is around 20% in wild populations (Cotton et al., 2014;Paczolt et al., 2017;Wilkinson et al., 2003). This pattern is unlike other species where drive males do poorly under sperm competition and the spread of drive is reliant on a high frequency of monandrous matings (Courret et al., 2019;Dyer and Hall, 2019;Price et al., 2008b). ...
In male X-linked meiotic drive systems, the driver causes degeneration of Y-bearing sperm, leading to female-biased offspring sex ratios. This potentially leads to a two-fold transmission advantage to drive chromosomes. However, drive-bearing sperm often do poorly in sperm competition, limiting their ability to spread. We use the stalk-eyed fly, Teleopsis dalmanni , to investigate the success of the X-linked Sex Ratio (SR) meiotic drive system. In this species, polyandrous matings, where a female mates with multiple males, are common. Recent findings demonstrate SR males transfer the same numbers of viable sperm as wildtype (ST) males during mating, implying that they do not necessarily have reduced fertility under sperm competition. Reciprocal mating trials were performed to measure the success of SR and ST sperm in double mated females, with either a SR or ST male mated first followed by a male of the alternative genotype. There was no significant difference in the number of offspring sired by SR and ST males. This equivalence held regardless of whether the SR male mated first or second. We show these results are consistent with previous studies that suggested SR male sperm do poorly in sperm competition. Future experiments will determine whether the competitive ability of SR males is maintained under higher stress conditions likely to be experienced in nature, in which females mate repeatedly with multiple males. The results from the current study helps to explain the high meiotic drive frequency of around 20% in wild populations in this species.
Impact Summary
Meiotic drive genes are selfish genetic elements that distort Mendelian patterns of inheritance to bias transmission in their favour. We use the stalk-eyed fly, Teleopsis dalmanni , to investigate the fitness effects associated with a meiotic drive gene called Sex Ratio (SR), which is linked to the X chromosome. In males, SR destroys Y-bearing sperm, meaning only X-bearing sperm are viable, and females who mate with drive males sire all-female broods. This confers a two-fold transmission advantage to the SR gene, as it is transmitted to all offspring.
We recently discovered that drive males have evolved compensatory mechanisms to cope with the sperm destruction caused by meiotic drive. They have greatly enlarged testes, allowing them to produce more sperm. When drive males mate with females, they deliver as many sperm and sire as many offspring as wildtype males. Building on this finding, we measured how drive male sperm performs against sperm from a non-carrier male in sperm competition – where the sperm from different males compete to fertilise an egg. Double mating trials were performed, where a single female was mated once to a drive and once to a non-carrier male. By genotyping offspring, we show that the number of offspring sired by the drive male was not different from the number sired by the non-carrier competitor.
These findings contrast with those in other species. Typically, drive males do poorly in sperm competition and their spread is severely restricted by sperm competition. In stalk-eyed flies, female multiple mating with many males is the norm, but this does not appear to inhibit the fertility of drive males. The success of drive under sperm competition helps to explain the high frequency of drive around 20% in natural populations of T. dalmanni .
... Nevertheless, our findings align with explicit investigations of male mating success conducted on the other well-known segregation distorters: SR elements in other Drosophila species [37,38] and the t haplotype in mice [39], with one notable exception. Female Teleopsis dalmanni stalk-eyed flies have been found to avoid mating with SR males [40,41]. In these systems, SR is genetically linked to a locus that affects eye-stalk width, a trait that is under sexual selection due to female choice [42]. ...
The Segregation Distorter ( SD ) allele found in Drosophila melanogaster distorts Mendelian inheritance in heterozygous males by causing developmental failure of non- SD spermatids, such that greater than 90% of the surviving sperm carry SD . This within-individual advantage should cause SD to fix, and yet SD is typically rare in wild populations. Here, we explore whether this paradox can be resolved by sexual selection, by testing if males carrying three different variants of SD suffer reduced pre- or post-copulatory reproductive success. We find that males carrying the SD allele are just as successful at securing matings as control males, but that one SD variant ( SD-5 ) reduces sperm competitive ability and increases the likelihood of female remating. We then used these results to inform a theoretical model; we found that sexual selection could limit SD to natural frequencies when sperm competitive ability and female remating rate equalled the values observed for SD-5 . However, sexual selection was unable to explain natural frequencies of the SD allele when the model was parameterized with the values found for two other SD variants, indicating that sexual selection alone is unlikely to explain the rarity of SD .
... The sexual ornament in T. dalmanni is also associated with sexratio meiotic drive (SR), a common type of selfish genetic element located on the X chromosome that causes selective destruction of Y-bearing sperm and the production of female-biased broods (Hurst & Pomiankowski, 1991;Jaenike, 2001;Lindholm et al., 2016). The X SR chromosome exists at moderate frequencies (~20%) in wild populations (Cotton et al., 2014;Paczolt et al., 2017;Wilkinson et al., 2003). Male carriers of X SR have reduced eyespan both under laboratory conditions Meade et al., 2019;Wilkinson et al., 1998) and in the wild (Cotton et al., 2014). ...
... The X SR chromosome exists at moderate frequencies (~20%) in wild populations (Cotton et al., 2014;Paczolt et al., 2017;Wilkinson et al., 2003). Male carriers of X SR have reduced eyespan both under laboratory conditions Meade et al., 2019;Wilkinson et al., 1998) and in the wild (Cotton et al., 2014). The drive and standard (X ST ) chromosomes are differentiated by a large paracentric inversion (or inversions; Johns et al., 2005), spanning at least one third of the chromosome (Paczolt et al., 2017). ...
... The X-linked QTL linked to meiotic drive explains over a third of the variation in male eyespan but just 9% of the variation in female eyespan . In wild flies, no association was found between female eyespan and ms395 allele size, a marker that is strongly associated with meiotic drive and male relative eyespan (Cotton et al., 2014). ...
Meiotic drive systems are associated with low frequency chromosomal inversions. These are expected to accumulate deleterious mutations due to reduced recombination and low effective population size. We test this prediction using the "sex-ratio" (SR) meiotic drive system of the Malaysian stalk-eyed fly Teleopsis dalmanni. SR is associated with a large inversion (or inversions) on the X chromosome. In particular, we study eyespan in males carrying the SR chromosome, as this trait is a highly exaggerated, sexually dimorphic trait, known to have heightened condition-dependent expression. Larvae were raised in low and high larval food stress environments. SR males showed reduced eyespan under the low and high stress treatments but there was no evidence of a condition-dependent decrease in eyespan under high stress. Similar but more complex patterns were observed for female eyespan, with evidence of additivity under low stress and heterosis under high stress. These results do not support the hypothesis that reduced sexual ornament size in meiotic drive males is due to a condition-dependent response to the putative increase in mutation load. Instead, reduced eyespan likely reflects compensatory resource allocation to different traits in response to drive-mediated destruction of sperm.
... In this species 10-30% of X chromosomes actively drive against the Y chromosome and result in carrier males producing 90% or more daughters (Presgraves et al. 1997). This sex ratio (SR) X chromosome causes an array of positive and negative impacts on fitness (Wilkinson et al. 2006;Finnegan et al. 2019;Meade et al. 2019) including reduced sexual ornament (eyespan) size in SR males (Wilkinson et al. 1998;Johns et al. 2005;Cotton et al. 2013). Based on a three locus comparison to an outgroup species, the SR X chromosome (X SR ) is old, having originated approximately 500 kya (Paczolt et al. 2017), and hundreds of mostly Xlinked genes are differentially expressed in SR males (Reinhardt et al. 2014). ...
Some stalk-eyed flies in the genus Teleopsis carry selfish genetic elements that induce sex ratio (SR) meiotic drive and impact the fitness of male and female carriers. Here, we produce a chromosome-level genome assembly of the stalk-eyed fly, T. dalmanni , to elucidate the pattern of genomic divergence associated with the presence of drive elements. We find evidence for multiple nested inversions along the sex ratio haplotype and widespread differentiation and divergence between the inversion types along the entire X chromosome. In addition, the genome contains tens of thousands of transposable element (TE) insertions and hundreds of transcriptionally active TE families that have produced new insertions. Moreover, we find that many TE families are expressed at a significantly higher level in SR male testis, suggesting a molecular connection between these two types of selfish genetic elements in this species. We identify T. dalmanni orthologs of genes involved in genome defense via the piRNA pathway, including core members maelstrom, piwi and Argonaute3 , that are diverging in sequence, expression or copy number between the SR and standard (ST) chromosomes, and likely influence TE regulation in flies carrying a sex ratio X chromosome.
... In Teleopsis dalmanni stalk-eyed flies carrying a sex ratio distorter (an X-linked meiotic driver), females prefer to mate with males with long eye-stalks. This signals that they carry a genetic suppressor of sex ratio drive meaning females will sire both sons and daughters (Cotton et al., 2014). On the other hand, in mice carrying an autosomal meiotic driver, the t-complex, heterozygous females avoid mating with males carrying the t-haplotype. ...
Selfish genetic elements (SGEs) such as replicating mobile elements, segregation distorters and maternally inherited endosymbionts, bias their transmission success relative to the rest of the genome to increase in representation in subsequent generations. As such, they generate conflict with the rest of the genome. Such intragenomic conflict is also a hallmark of sexually antagonistic (SA) alleles, which are shared genes between the sexes but that have opposing fitness effects when expressed in males and females. However, whilst both SGEs and SA alleles are recognized as common and potent sources of genomic conflict, the realization that SGEs can also generate sexually antagonistic selection and contribute to sexual conflict in addition to generate sexual selection is largely overlooked. Here, I show that SGEs frequently generate sex‐specific selection and outline how SGEs that are associated with compromised male fertility can shape female mating patterns, play a key role in the dynamics of sex‐determination systems and likely be an important source of sexually antagonistic genetic variation. Given the prevalence of SGEs, their contribution to sexual conflict is likely to be greatly overlooked.
... Female mate choice may additionally evolve in response to drive. In stalk-eyed flies, meiotic drive has been linked to small eye span, which may allow females to avoid mating with carrier males through assessing eye span (Wilkinson et al. 1998b;Cotton et al. 2014). Female house mice could avoid mating with drive males through detecting unique major histocompatibility alleles linked to the driving t complex (Silver 1985;Lindholm et al. 2013), although evidence remains unclear (Lindholm and Price 2016). ...
... Meiotic drive arose around 2-3.5 million years ago in the Teleopsis clade, and the X SR drive chromosome in T. dalmanni is estimated to have diverged from a nondriving ancestor (X ST ) around 1 million years ago (Swallow et al. 2005;Paczolt et al. 2017) and is characterized by a large inversion(s) covering most of the X chromosome Paczolt et al. 2017). X SR is found at appreciable frequencies (10%-30%) across populations and generations (Wilkinson et al. 2003;Cotton et al. 2014) but appears to lack genetic suppressors (Reinhold et al. 1999;Wolfenbarger and Wilkinson 2001;Paczolt et al. 2017). This means that there has been ample time and opportunity for adaptive responses to evolve in male carriers of the drive chromosome. ...
Selfish genetic elements that gain a transmission advantage through the destruction of sperm have grave implications for drive male fertility. In the X-linked SR meiotic drive system of a stalk-eyed fly, we found that drive males have greatly enlarged testes and maintain high fertility despite the destruction of half their sperm, even when challenged with fertilising large numbers of females. Conversely, we observed reduced allocation of resources to the accessory glands that probably explains the lower mating frequency of SR males. Body size and eyespan were also reduced, which are likely to impair viability and pre-copulatory success. We discuss the potential evolutionary causes of these differences between drive and standard males.
