Male eyespan size is associated with meiotic drive in wild stalk-eyed flies (Teleopsis dalmanni)

Cotton, Alison J.; Földvári, Mihály; Cotton, Samuel; Pomiankowski, Andrew

doi:10.1038/hdy.2013.131

Cited by 42 publications

(60 citation statements)

References 39 publications

(68 reference statements)

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“…Interestingly, the X-linked QTL was between ms395 and crc. Not only did this region also associate with sterility and sperm length (see below), but ms395 was also recently reported to be the best predictor of strong X drive in field-caught flies from the Gombak valley (Cotton et al 2014). This result suggests that ancestral and extant X drive factors may be located in the same region but have different sets of modifiers.…”

Section: Cryptic Drive and Extraordinary Sex Ratiosmentioning

confidence: 89%

“…90% or more female offspring occur at frequencies of 5-30% in the wild (Wilkinson et al 2003;Cotton et al 2014; K. Paczolt and J. Reinhardt, personal communication), which should generate strong selection as a consequence of biased sex ratios (Lande and Wilkinson 1999).…”

Section: Discussionmentioning

confidence: 99%

“…High frequencies of sex chromosome drive (Wilkinson et al 2003;Cotton et al 2014), reproductively isolated populations Swallow et al 2005;Rose et al 2014), and increasing availability of genomic resources (Baker et al 2009;Baker and Wilkinson 2010;Reinhardt et al 2014) make them also a tractable system for studying the genetic bases of reproductive isolation, such as those causing hybrid sterility. Our mapping results from two sets of interpopulation crosses suggest that genomic regions that influence sperm length also influence sterility and sex ratio.…”

Section: Discussionmentioning

confidence: 99%

“…Experimental crosses between flies from isolated populations of Teleopsis dalmanni and T. whitei in southeast Asia have revealed evidence for rapid evolution of male hybrid sterility and asymmetric gametic isolation (Rose et al 2014). These populations are also polymorphic for X chromosome meiotic drive in which carrier (or sex ratio, SR) males produce predominantly (.90%) female progeny (Presgraves et al 1997) and occur at frequencies of 10-30% (Wilkinson et al 2003;Cotton et al 2014). Recombination is rare or absent between X SR and X ST chromosomes , indicating that the extant drive system is in a paracentric inversion that involves most of the X chromosome (Christianson et al 2011).…”

mentioning

confidence: 99%

“…Most genes on the X in Teleopsis are on Muller element B, i.e., chromosome 2L in D. melanogaster , rather than the putative ancestral X-Muller element F (Vicoso and Bachtrog 2013), indicating that the sex chromosomes are independently derived in diopsids. Genes on the X influence sperm length (Johns and Wilkinson 2007), female sperm storage organ size , and eyestalk length (Wolfenbarger and Wilkinson 2001), with X SR and X ST males differing in eyespan in the lab (Wilkinson et al 1998;Johns et al 2005) and field (Cotton et al 2014). Consequently, drive-associated genes could influence hybrid fitness in multiple ways.…”

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confidence: 99%

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Haldane’s Rule Is Linked to Extraordinary Sex Ratios and Sperm Length in Stalk-Eyed Flies

et al. 2014

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We use three allopatric populations of the stalk-eyed fly Teleopsis dalmanni from Southeast Asia to test two predictions made by the sex chromosome drive hypothesis for Haldane's rule. The first is that modifiers that suppress or enhance drive should evolve rapidly and independently in isolated populations. The second is that drive loci or modifiers should also cause sterility in hybrid males. We tested these predictions by assaying the fertility of 2066 males derived from backcross experiments involving two pairs of populations and found that the proportion of mated males that fail to produce any offspring ranged from 38 to 60% among crosses with some males producing strongly female-biased or male-biased sex ratios. After genotyping each male at 25-28 genetic markers we found quantitative trait loci (QTL) that jointly influence male sterility, sperm length, and biased progeny sex ratios in each pair of populations, but almost no shared QTL between population crosses. We also discovered that the extant X SR chromosome has no effect on sex ratio or sterility in these backcross males. Whether shared QTL are caused by linkage or pleiotropy requires additional study. Nevertheless, these results indicate the presence of a "cryptic" drive system that is currently masked by suppressing elements that are associated with sterility and sperm length within but not between populations and, therefore, must have evolved since the populations became isolated, i.e., in ,100,000 years. We discuss how genes that influence sperm length may contribute to hybrid sterility.A major challenge to those who study speciation is to determine the causes of early reproductive isolation between incipient species. One avenue for gaining insight into this issue is to investigate the causes of Haldane's rule, i.e., the observation that the heterogametic sex of hybrid offspring are more likely to be sterile or inviable than the homogametic sex (Haldane 1922). This phenomenon has been observed in a wide range of animal taxa and is believed to be a nearly ubiquitous phase of early speciation (Orr 1997). Given that alleles for sterility or inviability are expected to be selected against within populations, models for the evolution of hybrid dysfunction typically assume two or more genes, each of which is neutral or advantageous within a population but have deleterious joint effects when mismatched between populations. Two nonmutually exclusive explanations (Turelli 1998) have been proposed for why these epistatic interactions, known as Dobzhansky-Muller incompatibilities (Dobzhansky 1937;Muller 1940Muller , 1942Orr 1995), should arise more quickly in the heterogametic sex.The dominance hypothesis (Muller 1942;Orr 1993;Turelli and Orr 1995) assumes that if genes causing hybrid dysfunction are recessive, then the heterogametic sex will be affected more than the homogametic sex. This result is expected because the degenerate (or missing, in XO taxa) sex chromosome possessed by the heterogametic sex fails to mask recessive alleles present on it...

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Section: Cryptic Drive and Extraordinary Sex Ratiosmentioning

confidence: 89%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Haldane’s Rule Is Linked to Extraordinary Sex Ratios and Sperm Length in Stalk-Eyed Flies

et al. 2014

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Proximal fate marker homothorax marks the lateral extension of stalk‐eyed fly Cyrtodopsis whitei

Singh

Gogia

Chang

et al. 2019

Genesis

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The placement of eyes on insect head is an important evolutionary trait. The stalk-eyed fly, Cyrtodopsis whitei, exhibits a hypercephaly phenotype where compound eyes are located on lateral extension from the head while the antennal segments are placed inwardly on this stalk. This stalk-eyed phenotype is characteristic of the family Diopsidae in the Diptera order and dramatically deviates from other dipterans, such as Drosophila.Like other insects, the adult eye and antenna of stalk-eyed fly develop from a complex eye-antennal imaginal disc. We analyzed the markers involved in proximo-distal (PD) axis of the developing eye imaginal disc of the stalk-eyed flies. We used homothorax (hth) and distalless (dll), two highly conserved genes as the marker for proximal and distal fate, respectively. We found that lateral extensions between eye and antennal field of the stalk-eyed fly's eye-antennal imaginal disc exhibit robust Hth expression. Hth marks the head specific fate in the eye-and proximal fate in the antenna-disc. Thus, the proximal fate marker Hth expression evolves in the stalk-eyed flies to generate lateral extensions for the placement of the eye on the head. Moreover, during pupal eye metamorphosis, the lateral extension folds back on itself to place the antenna inside and the adult compound eye on the distal tip. Interestingly, the compound eye in other insects does not have a prominent PD axis as observed in the stalk-eyed fly. K E Y W O R D S dacshund, distalless, Drosophila, eye development, eye-antennal imaginal disc, homothorax, proximo-distal axis, stalk-eyed fly

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The suppression of a selfish genetic element increases a male's mating success in a fly

Lyth,

Betancourt,

Price

et al. 2023

Ecology and Evolution

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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.

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Male eyespan size is associated with meiotic drive in wild stalk-eyed flies (Teleopsis dalmanni)

Cited by 42 publications

References 39 publications

Haldane’s Rule Is Linked to Extraordinary Sex Ratios and Sperm Length in Stalk-Eyed Flies

Haldane’s Rule Is Linked to Extraordinary Sex Ratios and Sperm Length in Stalk-Eyed Flies

Proximal fate marker homothorax marks the lateral extension of stalk‐eyed fly Cyrtodopsis whitei

The suppression of a selfish genetic element increases a male's mating success in a fly

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