scholarly journals Driven to Extinction: On the Probability of Evolutionary Rescue from Sex-Ratio Meiotic Drive

2015 ◽  
Author(s):  
Robert Unckless ◽  
Andrew Clark

Many evolutionary processes result in sufficiently low mean fitness that they pose a risk of species extinction. Sex-ratio meiotic drive was recognized by W.D. Hamilton (1967) to pose such a risk, because as the driving sex chromosome becomes common, the opposite sex becomes rare. We expand on Hamilton’s classic model by allowing for the escape from extinction due to evolution of suppressors of X and Y drivers. We explore differences in the two systems in their probability of escape from extinction. Several novel conclusions are evident, including a) that extinction time scales approximately with the log of population size so that even large populations may go extinct quickly, b) extinction risk is driven by the relationship between female fecundity and drive strength, c) anisogamy and the fact that X and Y drive result in sex ratios skewed in opposite directions, mean systems with Y drive are much more likely to go extinct than those with X drive, and d) suppressors are most likely to become established when the strength of drive is intermediate, since weak drive leads to weak selection for suppression and strong drive leads to rapid extinction.


Genetics ◽  
1997 ◽  
Vol 147 (3) ◽  
pp. 1169-1180 ◽  
Author(s):  
Daven C Presgraves ◽  
Emily Severance ◽  
Gerald S Willrinson

Meiotically driven sex chromosomes can quickly spread to fixation and cause population extinction unless balanced by selection or suppressed by genetic modifiers. We report results of genetic analyses that demonstrate that extreme female-biased sex ratios in two sister species of stalk-eyed flies, Cyrtodiopsis dalmanni and C. whitei, are due to a meiotic drive element on the X chromosome (Xd). Relatively high frequencies of Xd in C. dalmanni and C. whitei (13–17% and 29%, respectively) cause female-biased sex ratios in natural populations of both species. Sex ratio distortion is associated with spermatid degeneration in male carriers of Xd. Variation in sex ratios is caused by Y-linked and autosomal factors that decrease the intensity of meiotic drive. Y-linked polymorphism for resistance to drive exists in C. dalmanni in which a resistant Y chromosome reduces the intensity and reverses the direction of meiotic drive. When paired with Xd, modifying Y chromosomes (Ym) cause the transmission of predominantly Y-bearing sperm, and on average, production of 63% male progeny. The absence of sex ratio distortion in closely related monomorphic outgroup species suggests that this meiotic drive system may predate the origin of C. whitei and C. dalmanni. We discuss factors likely to be involved in the persistence of these sex-linked polymorphisms and consider the impact of Xd on the operational sex ratio and the intensity of sexual selection in these extremely sexually dimorphic flies.



2016 ◽  
Vol 113 (15) ◽  
pp. 4110-4115 ◽  
Author(s):  
Quentin Helleu ◽  
Pierre R. Gérard ◽  
Raphaëlle Dubruille ◽  
David Ogereau ◽  
Benjamin Prud’homme ◽  
...  

Sex chromosome meiotic drive, the non-Mendelian transmission of sex chromosomes, is the expression of an intragenomic conflict that can have extreme evolutionary consequences. However, the molecular bases of such conflicts remain poorly understood. Here, we show that a young and rapidly evolving X-linked heterochromatin protein 1 (HP1) gene, HP1D2, plays a key role in the classical Paris sex-ratio (SR) meiotic drive occurring in Drosophila simulans. Driver HP1D2 alleles prevent the segregation of the Y chromatids during meiosis II, causing female-biased sex ratio in progeny. HP1D2 accumulates on the heterochromatic Y chromosome in male germ cells, strongly suggesting that it controls the segregation of sister chromatids through heterochromatin modification. We show that Paris SR drive is a consequence of dysfunctional HP1D2 alleles that fail to prepare the Y chromosome for meiosis, thus providing evidence that the rapid evolution of genes controlling the heterochromatin structure can be a significant source of intragenomic conflicts.



Genetics ◽  
1991 ◽  
Vol 128 (4) ◽  
pp. 841-858 ◽  
Author(s):  
L D Hurst ◽  
A Pomiankowski

Abstract Unisexual hybrid disruption can be accounted for by interactions between sex ratio distorters which have diverged in the species of the hybrid cross. One class of unisexual hybrid disruption is described by Haldane's rule, namely that the sex which is absent, inviable or sterile is the heterogametic sex. This effect is mainly due to incompatibility between X and Y chromosomes. We propose that this incompatibility is due to a mutual imbalance between meiotic drive genes, which are more likely to evolve on sex chromosomes than autosomes. The incidences of taxa with sex chromosome drive closely matches those where Haldane's rule applies: Aves, Mammalia, Lepidoptera and Diptera. We predict that Haldane's rule is not universal but is correct for taxa with sex chromosome meiotic drive. A second class of hybrid disruption affects the male of the species regardless of which sex is heterogametic. Typically the genes responsible for this form of disruption are cytoplasmic. These instances are accounted for by the release from suppression of cytoplasmic sex ratio distorters when in a novel nuclear cytotype. Due to the exclusively maternal transmission of cytoplasm, cytoplasmic sex ratio distorters cause only female-biased sex ratios. This asymmetry explains why hybrid disruption is limited to the male.



Genetics ◽  
2000 ◽  
Vol 154 (2) ◽  
pp. 687-694 ◽  
Author(s):  
Emmanouil T Dermitzakis ◽  
John P Masly ◽  
Heidi M Waldrip ◽  
Andrew G Clark

Abstract Interspecific hybrids and backcrossed organisms generally suffer from reduced viability and/or fertility. To identify and genetically map these defects, we introgressed regions of the Drosophila sechellia genome into the D. simulans genome. A female-biased sex ratio was observed in 24 of the 221 recombinant inbred lines, and subsequent tests attributed the skew to failure of Y-bearing sperm to fertilize the eggs. Apparently these introgressed lines fail to suppress a normally silent meiotic drive system. Using molecular markers we mapped two regions of the Drosophila genome that appear to exhibit differences between D. simulans and D. sechellia in their regulation of sex chromosome segregation distortion. The data indicate that the sex ratio phenotype results from an epistatic interaction between at least two factors. We discuss whether this observation is relevant to the meiotic drive theory of hybrid male sterility.



Genetics ◽  
2000 ◽  
Vol 154 (1) ◽  
pp. 229-236
Author(s):  
Michel Cazemajor ◽  
Dominique Joly ◽  
Catherine Montchamp-Moreau

Abstract The sex-ratio trait, an example of naturally occurring X-linked meiotic drive, has been reported in a dozen Drosophila species. Males carrying a sex-ratio X chromosome produce an excess of female offspring caused by a deficiency of Y-bearing sperm. In Drosophila simulans, such males produce ~70–90% female offspring, and 15–30% of the male offspring are sterile. Here, we investigate the cytological basis of the drive in this species. We show that the sex-ratio trait is associated with nondisjunction of Y chromatids in meiosis II. Fluorescence in situ hybridization (FISH) using sex-chromosome-specific probes provides direct evidence that the drive is caused by the failure of the resulting spermatids to develop into functional sperm. XYY progeny were not observed, indicating that few or no YY spermatids escape failure. The recovery of XO males among the progeny of sex-ratio males shows that some nullo-XY spermatids become functional sperm and likely explains the male sterility. A review of the cytological data in other species shows that aberrant behavior of the Y chromosome may be a common basis of sex-ratio meiotic drive in Drosophila and the signal that triggers differential spermiogenesis failure.



Genetics ◽  
1981 ◽  
Vol 98 (2) ◽  
pp. 317-334
Author(s):  
Terrence W Lyttle

ABSTRACT Laboratory populations of Drosophila melanogaster were challenged by pseudo-Y drive, which mimics true Y-chromosome meiotic drive through the incorporation of Segregation Distorter (SD) in a T(Y;2) complex. This causes extreme sex-ratio distrotion and can ultimately lead to population extinction. Populations normally respond by the gradual accumulation of drive suppressors, and this reduction in strength of distortion allows the sex ratio to move closer to the optimal value of 1:1. One population monitored, however, was rapidly able to neutralize the effects of sex-ratio distortion by the accumulation of sex-chromosome aneuploids (XXY, XYY). This apparently occurs because XX-bearing eggs, produced in relatively high numbers (~4%) by XXY genotypes, become the main population source of females under strong Y-chromosome drive. Computer simulation for a discrete generation model incorporating random mating with differences in fitness and segregation permits several predictions that can be compared to the data. First, sex-chromosome aneuploids should rapidly attain equilibrium, while stabilizing the population at ~60% males. This sex ratio should be roughly independent of the strength of the meiotic drive. Moreover, conditions favoring the accumulation of drive suppressors (e.g., weak distortion, slow population extinction) are insufficient for maintaining aneuploidy, while conditions favoring aneuploidy (e.g., strong distortion, low production of females) lead to population extinction before drive suppressors can accumulate. Thus, the different mechanisms for neutralizing sex-ratio distortion are complementary. In addition, Y drive and sex-chromosome aneuploidy are potentially co-adaptive, since under some conditions neither will survive alone. Finally, these results suggest the possibility that genetic variants promoting sex-chromosome nondisjunction may have a selective advantage in natural populations faced with sex-ratio distortion.



Genetics ◽  
1998 ◽  
Vol 149 (1) ◽  
pp. 143-155 ◽  
Author(s):  
Bruce D McKee ◽  
Kathy Wilhelm ◽  
Cynthia Merrill ◽  
Xiao-jia Ren

Abstract In Drosophila melanogaster, deletions of the pericentromeric X heterochromatin cause X-Y nondisjunction, reduced male fertility and distorted sperm recovery ratios (meiotic drive) in combination with a normal Y chromosome and interact with Y-autosome translocations (T(Y;A)) to cause complete male sterility. The pericentromeric heterochromatin has been shown to contain the male-specific X-Y meiotic pairing sites, which consist mostly of a 240-bp repeated sequence in the intergenic spacers (IGS) of the rDNA repeats. The experiments in this paper address the relationship between X-Y pairing failure and the meiotic drive and sterility effects of Xh deletions. X-linked insertions either of complete rDNA repeats or of rDNA fragments that contain the IGS were found to suppress X-Y nondisjunction and meiotic drive in Xh−/Y males, and to restore fertility to Xh−/T(Y;A) males for eight of nine tested Y-autosome translocations. rDNA fragments devoid of IGS repeats proved incapable of suppressing either meiotic drive or chromosomal sterility. These results indicate that the various spermatogenic disruptions associated with X heterochromatic deletions are all consequences of X-Y pairing failure. We interpret these findings in terms of a novel model in which misalignment of chromosomes triggers a checkpoint that acts by disabling the spermatids that derive from affected spermatocytes.



Genetics ◽  
2002 ◽  
Vol 160 (4) ◽  
pp. 1721-1731 ◽  
Author(s):  
Jesse E Taylor ◽  
John Jaenike

AbstractSeveral empirical studies of sperm competition in populations polymorphic for a driving X chromosome have revealed that Sex-ratio males (those carrying a driving X) are at a disadvantage relative to Standard males. Because the frequency of the driving X chromosome determines the population-level sex ratio and thus alters male and female mating rates, the evolutionary consequences of sperm competition for sex chromosome meiotic drive are subtle. As the SR allele increases in frequency, the ratio of females to males also increases, causing an increase in the male mating rate and a decrease in the female mating rate. While the former change may exacerbate the disadvantage of Sex-ratio males during sperm competition, the latter change decreases the incidence of sperm competition within the population. We analyze a model of the effects of sperm competition on a driving X chromosome and show that these opposing trends in male and female mating rates can result in two coexisting locally stable equilibria, one corresponding to a balanced polymorphism of the SR and ST alleles and the second to fixation of the ST allele. Stochastic fluctuations of either the population sex ratio or the SR frequency can then drive the population away from the balanced polymorphism and into the basin of attraction for the second equilibrium, resulting in fixation of the SR allele and extinction of the population.



Plant Ecology ◽  
2008 ◽  
Vol 200 (2) ◽  
pp. 229-240 ◽  
Author(s):  
Grzegorz Iszkuło ◽  
Anna K. Jasińska ◽  
Marian J. Giertych ◽  
Adam Boratyński


2021 ◽  
Author(s):  
Jeffrey Vedanayagam ◽  
Ching-Jung Lin ◽  
Eric C. Lai

Meiotic drivers are a class of selfish genetic elements that are widespread across eukaryotes. Their activities are often detrimental to organismal fitness and thus trigger drive suppression to ensure fair segregation during meiosis. Accordingly, their existence is frequently hidden in genomes, and their molecular functions are little known. Here, we trace evolutionary steps that generated the Dox meiotic drive system in Drosophila simulans (Dsim), which distorts male:female balance (sex-ratio) by depleting male progeny. We show that Dox emerged via stepwise mobilization and acquisition of portions of multiple D. melanogaster genes, including the sperm chromatin packaging gene protamine. Moreover, we reveal novel Dox homologs in Dsim and massive, recent, amplification of Dox superfamily genes specifically on X chromosomes of its closest sister species D. mauritiana (Dmau) and D. sechellia (Dsech). The emergence of Dox superfamily genes is tightly associated with 1.688 family satellite repeats that flank de novo genomic copies. In concert, we find coordinated emergence and diversification of autosomal hairpin RNA/siRNAs loci that target subsets of Dox superfamily genes across simulans clade species. Finally, an independent set of protamine amplifications the Y chromosome of D. melanogaster indicates that protamine genes are frequent and recurrent players in sex chromosome dynamics. Overall, we reveal fierce genetic arms races between meiotic drive factors and siRNA suppressors associated with recent speciation.



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