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Frequency change per generation for a rare female choice allele A c (frequency of choice 5 10 75 ) when preference is based on Y-linked drive resistance (¢lled triangles) (preference of males with allele Y m against males with Y ), autosomal drive resistance (open triangles) (preference of males with allele R m against males with R ), and the meiotic drive locus (¢lled squares) (preference of males with allele X against males with X d ). For values with a relative female preference smaller than one, females are assumed to avoid mating with the respective males and thus mate preferentially with males having the alternative allele. For the ¢gured cases, moderate costs of drive and resistance were assumed ( f c 0.3). Similar changes in the frequency A c resulted for all values of f and c that led to a polymorphism between X d and Y m .
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As a special version of the good-genes hypothesis, it was recently proposed that females could benefit from choosing drive-resistant males in a meiotic drive system. Here, we examine with a three-locus, six-allele population genetic model whether female choice for drive resistance can evolve. An allele leading to female preference for drive-resista...
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... Models are employed in the sciences for many reasons, and fall within a biological abstraction continuum (Servedio et al., 2014), going from fully verbal, highly abstract models (e.g., Van Valen 1973), through proof-of-concept models that formalize verbal models (e.g., Maynard Smith 1978;Reinhold et al. 1999), to models that interact directly with data through explicit mathematical functions (Yule, 1924;Felsenstein, 1973;Hasegawa et al., 1985;Hudson, 1990). ...
Biology has become a highly mathematical discipline in which probabilistic models play a central role. As a result, research in the biological sciences is now dependent on computational tools capable of carrying out complex analyses. These tools must be validated before they can be used, but what is understood as validation varies widely among methodological contributions. This may be a consequence of the still embryonic stage of the literature on statistical software validation for computational biology. Our manuscript aims to advance this literature. Here, we describe and illustrate good practices for assessing the correctness of a model implementation, with an emphasis on Bayesian methods. We also introduce a suite of functionalities for automating validation protocols. It is our hope that the guidelines presented here help sharpen the focus of discussions on (as well as elevate) expected standards of statistical software for biology.
... SGEs are near ubiquitous in nature (Hurst & Werren, 2001) and include transposable elements, homing endonucleases, and meiotic drivers; endosymbionts, although they can be beneficial to their hosts, can also share characteristics of SGEs. SGEs are often costly to the individuals who carry them and so there is a benefit for females to evolve mating behavior that will disfavor SGE-bearing males (Lande & Wilkinson, 1999;Lindholm et al., 2016;Reinhold et al., 1999;Tregenza & Wedell, 2000). Genetic suppressors are a common evolutionary response to SGEs and endosymbionts (Bastide et al., 2011;Hornett et al., 2006Hornett et al., , 2008Tao et al., 2007;Verspoor et al., 2018Verspoor et al., , 2020. ...
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.
... Indeed, for some naturally occurring gene drives, species have evolved to avoid mating with drive carriers if they can be reliably detected through a specific trait (Lenington, 1991;Wilkinson et al., 1998). Despite having theoretical support (Lande & Wilkinson, 1999;Manser, Lindholm, & Weissing, 2017;Reinhold et al., 1999), empirical evidence for mate avoidance of natural drive carriers is limited . Whether a population could evolve to detect and behaviourally reduce transmission of a synthetic gene drive thus remain largely unknown. ...
Gene drive technology, in which fast‐spreading engineered drive alleles are introduced into wild populations, represents a promising new tool in the fight against vector‐borne diseases, agricultural pests and invasive species. Due to the risks involved, gene drives have so far only been tested in laboratory settings while their population‐level behaviour is mainly studied using mathematical and computational models. The spread of a gene drive is a rapid evolutionary process that occurs over timescales similar to many ecological processes. This can potentially generate strong eco‐evolutionary feedback that could profoundly affect the dynamics and outcome of a gene drive release. We, therefore, argue for the importance of incorporating ecological features into gene drive models. We describe the key ecological features that could affect gene drive behaviour, such as population structure, life‐history, environmental variation and mode of selection. We review previous gene drive modelling efforts and identify areas where further research is needed. As gene drive technology approaches the level of field experimentation, it is crucial to evaluate gene drive dynamics, potential outcomes, and risks realistically by including ecological processes.
... One of the best-known ideas is that noncarriers may avoid drive carriers as mates, preventing offspring from inheriting harmful drivers and improving offspring fitness. Theoretical models support this idea (Lande & Wilkinson, 1999;Manser et al., 2017;Randerson et al., 2000;Reinhold et al., 1999). However, this requires a trait that reliably reveals the presence or absence of drive (Lande & Wilkinson, 1999;Manser et al., 2017). ...
Scientists are rapidly developing synthetic gene drive elements intended for release into natural populations. These are intended to control or eradicate disease vectors and pests, or to spread useful traits through wild populations for disease control or conservation purposes. However, a crucial problem for gene drives is the evolution of resistance against them, preventing their spread. Understanding the mechanisms by which populations might evolve resistance is essential for engineering effective gene drive systems. This review summarizes our current knowledge of drive resistance in both natural and synthetic gene drives. We explore how insights from naturally occurring and synthetic drive systems can be integrated to improve the design of gene drives, better predict the outcome of releases and understand genomic conflict in general.
... However, subsequent work has not confirmed the presence of suppressors on either the Y or the autosomes . Furthermore, modelling suggest that preference for Y-linked suppression cannot evolve (Reinhold et al. 1999). This is because Y-linked suppressors must come at a cost, or else they would spread to fixation and drive would be undetectable. ...
Meiotic drive is a type of selfish genetic element that, in heterozygous males, disables or destroys non-carrier sperm in order to bias its own transmission. Meiotic drive genes are predicted to spread rapidly due to this transmission advantage and even, if sex-linked, cause population extinction due to the loss of one sex. Despite this, many meiotic drive genes are found at low/moderate, stable frequencies, which implies their carriers must bear unknown costs that balance this transmission advantage. Such costs may come about as direct or pleiotropic effects of the meiotic drive gene(s) themselves, or because drive is often associated with inversions that are expected to accumulate deleterious mutations. The theme of the thesis has been to search for costs of meiotic drive in the Malaysian stalk-eyed fly, Teleopsis dalmanni. First, I assess whether the expected low quality of meiotic drive males has impacted the strength of their mate preference for high quality females. I find that male mate preference does not depend on drive status but does depend on eyespan. Male eyespan is a sexually- selected ornamental trait and drive males typically have small eyespan. I also show that drive males are unable to mate as frequently as non-drive males. Second, I study the effect of meiotic drive on the egg-to-adult viability of stalk-eyed flies. I show that drive reduces the viability of both sexes, with drive males and homozygous drive females showing the greatest loss of 5 viability compared to their non-drive counterparts. Third, I study the effect of larval food stress on the drive-associated reduction in male eyespan. I find that drive males and females have reduced eyespan, but the magnitude of this reduction does not increase under high stress. This implies that the small eyespan of drive males is unlikely to be a condition-dependent effect of the expected increased mutation load. I discuss how small eyespan may instead be part of a suite of adaptations to maintain high fertility in the face of the destruction of half of all sperm. Finally, I use experimental evolution to track the frequency of meiotic drive in cage populations and find considerable heterogeneity. While one cage is driven extinct due to the loss of males, drive frequency generally declines in other populations, disappearing entirely from some after six generations.
... 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.
... However, further work addressing this found no effect of the Y chromosome on relative eyespan (eyespan after variation in thorax size is taken into account) (Wolfenbarger and Wilkinson, 2001), and this hypothesis is not supported by theory, which suggests that when resistance is Y-linked, female choice for driveresistant males is disadvantageous (Reinhold et al., 1999). Further work has failed to find clear evidence for drive suppression in T. dalmanni Paczolt et al., 2017). ...
... The drive system in T. dalmanni is relatively ancient at around 500,000 years since the divergence of X ST and X SR (Paczolt et al., 2017), so there has been ample time for an adaptive response to evolve, but no clear evidence of autosomal suppression. Y-linked suppressors have been suggested Wilkinson et al., 1998b), however later work has not found any evidence for suppression in this species (Reinhold et al., 1999;Wolfenbarger and Wilkinson, 2001;Paczolt et al., 2017). Evidence for suppression has been found in many systems (Stalker, 1961;Tokuyasu et al., 1977;Gummere et al., 1986;Hauschteck-Jungen, 1990;Wood and Newton, 1991;Carvalho and Klaczko, 1993;Carvalho et al., 1997;Cazemajor et al., 1997;Atlan et al., 2003;Tao et al., 2007b), but it is not the rule as no evidence of suppressors has been uncovered in D. pseudoobscura or D. neotestacea (Dyer, 2012). ...
... In some cases, suppressors appear to spread to fixation and can entirely mask the underlying activity of drive elements, that are revealed through crosses with naïve populations (Dermitzakis et al., 2000;Tao et al., 2001). However, segregating suppressors are not an inevitable feature of drive systems, as they appear to be lacking in a range of species, including D. pseudoobscura, D. neotestacea, D. recens (Dyer et al., 2007;Dyer, 2012), as well as stalk-eyed flies (Reinhold et al., 1999;Wolfenbarger and Wilkinson, 2001;Paczolt et al., 2017). ...
Meiotic drive genes are a class of segregation distorter that gain a transmission advantage in heterozygous males by causing degeneration of non-carrier sperm. This advantage must be balanced by fertility or viability costs if drive is to remain at stable frequencies in a population. A reduction in male fertility due to sperm destruction reduces the fitness of the rest of the genome, accordingly mechanisms to circumvent the effects of drive may evolve. Such adaptations will have implications for how likely it is that drive will persist. The primary theme of this thesis has been examining fertility consequences of meiotic drive in a Malaysian stalk-eyed fly, Teleopsis dalmanni. I demonstrate that drive carrier males are not sperm limited, despite the destruction of half their sperm. They produce ejaculates with sperm numbers equivalent to wildtype male ejaculates. Furthermore, drive males achieve this with greatly enlarged testes. However, resources are not unlimited; drive males also have reduced body size, and reduced accessory glands and eyespan for their body size. Accessory gland size limits male mating frequency, and male eyespan is a sexually selected trait used in female choice and male-male competition. I discuss how these patters fit with theoretical models that predict males should invest in producing an optimal ejaculate according to levels of expected sperm competition, even if they are low-fertility males. A second interrelated theme of this thesis has been to examine the benefits of polyandry, female mating with multiple males, using wild-caught individuals. Polyandry is widespread across many taxa and almost ubiquitous in insects. However, there is much debate around its proximate and ultimate causes. There are many costs associated with mating and so polyandry requires an adaptive explanation. I utilise data on wild-caught T. dalmanni to explore how natural variation amongst females and males influences fertility gains for females.
... Motivated by the stalk-eyed fly system (Wilkinson et al. 1998), two models investigated possible interactions between female choice and a sex-linked distorter. Reinhold et al. (1999) consider female choice for a distortion suppressor. The model suggests that, unexpectedly, female preferences in favor of a distortion suppressor is always selected against. ...
... Our findings are consistent with the few previous models addressing mate choice evolution in the presence of distorters, all focusing on different types of sex-linked distorters (Lande and Wilkinson 1999;Reinhold et al. 1999;Randerson et al. 2000). In the case of sex-linked distortion, choice benefits stem from the fact that mating with a distorter-free partner will result in offspring of even sex ratio. ...
... The conclusions are similar to the ones presented here: cost-free (Lande and Wilkinson 1999) and costly (Randerson et al. 2000) mate choice for distorter/male-killer-free mates can stably persist. Mate choice for drive suppression, on the other hand, seems not beneficial (Reinhold et al. 1999). Despite these similarities, there may be quantitative differences between autosomal and sex-linked distorters. ...
The evolution of female preference for male genetic quality remains a controversial topic in sexual selection research. One well-known problem, known as the lek paradox, lies in understanding how variation in genetic quality is maintained in spite of natural selection and sexual selection against low-quality alleles. Here, we theoretically investigate a scenario where females pay a direct fitness cost to avoid males carrying an autosomal segregation distorter. We show that preference evolution is greatly facilitated under such circumstances. Because the distorter is transmitted in a non-Mendelian fashion, it can be maintained in the population despite directional sexual selection. The preference helps females avoid fitness costs associated with the distorter. Interestingly, we find that preference evolution is limited if the choice allele induces a very strong preference or if distortion is very strong. Moreover, the preference can only persist in the presence of a signal that reliably indicates a male's distorter genotype. Hence, even in a system where the lek paradox does not play a major role, costly preferences can only spread under specific circumstances. We discuss the importance of distorter systems for the evolution of costly female choice and potential implications for the use of artificial distorters in pest control. This article is protected by copyright. All rights reserved
... Due to the complete inviability of t/t-homozygotes, t/+-heterozygous females may lose up to 50% of their offspring depending on the strength of drive. One way for females to escape this would be to avoid t/+males as mates and instead mate preferentially with wild-type males (Reinhold, Engqvist, Misof, & Kurtz, 1999). Yet, it may be difficult to Received: 21 July 2017 Nevertheless, the element is still driving, as the proportion of offspring fertilized by driving sperm is higher than the expected 25%. ...
Sex is good for us, but it is a compromise. For the benefit of being able to produce genetically variable offspring, we must pay the cost of passing on only half our genes to each of them. Whilst evolutionary biologists still puzzle over the precise details of why the benefits of sex so frequently seem to outweigh the costs (Neiman, Lively, & Meirmans, 2017), one major challenge to sexual reproduction is the fact that if we pass on only half our genetic material to each gamete, there is a strong incentive for each individual allele to try to gain an unfair representation during gamete production. Fundamental to stabilizing sex once it evolves is therefore the ability to ensure a fair meiosis. Nevertheless, this system is not perfect, and some selfish genetic elements – so-called meiotic drivers – manage to tip the meiotic scales in their favour and gain a transmission advantage (review in Burt and Trivers, 2006). In this issue of Molecular Ecology, Manser, Lindholm, Simmons, and Firman (2017) demonstrate that in house mice, the effectiveness of one such harmful transmission distorter is reduced by polyandry and hence that population viability can be somewhat restored by female promiscuity.
... Both verbal intuition and preliminary evidence led the research group to propose that females preferred males with long eyestalks because this exaggerated trait resided on a Y chromosome that was resistant to an X chromosome driver with biased transmission [45]. However, a proof-ofconcept model highlighted the flawed logic of this verbal model; the mathematical model showed that females choosing to mate with males bearing a drive-resistant Y chromosome (as putatively indicated by long eyestalks) would have lower fitness than nonchoosy females, and therefore this preference would not evolve [46]. In contrast, female choice for long eyestalks could be favored if long eyestalks were genetically associated with a nondriving allele at the (Xlinked) drive locus [46], so long as the eyestalk-length and drive loci were tightly linked [47]. ...
... However, a proof-ofconcept model highlighted the flawed logic of this verbal model; the mathematical model showed that females choosing to mate with males bearing a drive-resistant Y chromosome (as putatively indicated by long eyestalks) would have lower fitness than nonchoosy females, and therefore this preference would not evolve [46]. In contrast, female choice for long eyestalks could be favored if long eyestalks were genetically associated with a nondriving allele at the (Xlinked) drive locus [46], so long as the eyestalk-length and drive loci were tightly linked [47]. These proof-of-concept models provided a new direction for empirical work, leading to the collection of new evidence demonstrating that the X-driver is linked to the eyestalk-length locus by an inversion [48], with the nondriver and long eyestalk in coupling phase (i.e., on the same haplotype). ...
Progress in science often begins with verbal hypotheses meant to explain why certain biological phenomena exist. An important purpose of mathematical models in evolutionary research, as in many other fields, is to act as “proof-of-concept” tests of the logic in verbal explanations, paralleling the way in which empirical data are used to test hypotheses. Because not all subfields of biology use mathematics for this purpose, misunderstandings of the function of proof-of-concept modeling are common. In the hope of facilitating communication, we discuss the role of proof-of-concept modeling in evolutionary biology.
