An X chromosome effect responsible for asymmetric reproductive isolation between male Drosophila virilis and heterospecific females

Genome ◽  
2009 ◽  
Vol 52 (1) ◽  
pp. 49-56 ◽  
Author(s):  
Desirée Nickel ◽  
Alberto Civetta

Reproductive isolation between closely related species is expressed through uncoordinated courtship, failed fertilization, and (or) postzygotic barriers. Behavioural components of mating often form an initial barrier to hybridization between species. In many animals, females are responsible for mating discrimination in both intra- and interspecific crosses; males of Drosophila virilis group represent an exception to this trend. Using overall productivity tests, we show that a lower proportion of D. virilis males sire progeny when paired with a heterospecific female ( Drosophila novamexicana or Drosophila americana texana ) for 2 weeks. This suggests male mate discrimination or some other kind of asymmetrical incompatibility in courtship and mating or early zygote mortality. We used males from D. virilis – D. novamexicana and from D. virilis – D. a. texana backcross populations to map chromosome effects responsible for male reproductive isolation. Results from the analysis of both backcross male populations indicate a major X chromosome effect. Further, we conduct a male behavioural analysis to show that D. virilis males significantly fail to continue courtship after the first step of courtship, when they tap heterospecific females. The combined results of a major X chromosome effect and the observation that D. virilis males walk away from females after tapping suggest that future studies should concentrate on the identification of X-linked genes affecting the ability of males to recognize conspecific females.

Genetics ◽  
1989 ◽  
Vol 121 (3) ◽  
pp. 527-537 ◽  
Author(s):  
H A Orr ◽  
J A Coyne

Abstract In a genetic study of postzygotic reproductive isolation among species of the Drosophila virilis group, we find that the X chromosome has the largest effect on male and female hybrid sterility and inviability. The X alone has a discernible effect on postzygotic isolation between closely related species. Hybridizations involving more distantly related species also show large X-effects, although the autosomes may also play a role. In the only hybridization yet subjected to such analysis, we show that hybrid male and female sterility result from the action of different X-linked loci. Our results accord with genetic studies of other taxa, and support the view that both Haldane's rule (heterogametic F1 sterility or inviability) and the large effect of the X chromosome on reproductive isolation result from the accumulation by natural selection of partially recessive or underdominant mutations. We also describe a method that allows genetic analysis of reproductive isolation between species that produce completely sterile or inviable hybrids. Such species pairs, which represent the final stage of speciation, cannot be analyzed by traditional methods. The X chromosome also plays an important role in postzygotic isolation between these species.


2019 ◽  
Author(s):  
Dean M. Castillo ◽  
Leonie C. Moyle

AbstractAlthough observed in many interspecific crosses, the genetic basis of most hybrid incompatibilities is still unknown. Mismatches between parental genomes in selfish elements and the genes that regulate these elements are frequently hypothesized to underlie hybrid dysfunction. We evaluated the potential role of transposable elements (TEs) in hybrid incompatibilities by examining hybrids between Drosophila virilis strains polymorphic for TEs that cause dysgenesis and a closely related species that appears to lack these elements. Using genomic data, we confirmed copy number differences in potentially causal TEs between the dysgenic-causing D. virilis (TE+) strain and a sensitive D. virilis (TE-) strain and D. lummei genotype. We then contrasted isolation phenotypes in a cross where dysgenic TEs are absent from both D. virilis (TE-) and D. lummei parental genotypes, to a cross where dysgenic TEs are present in the D. virilis (TE+) parent and absent in the D. lummei parent, predicting increased reproductive isolation in the latter cross. Using F1 and backcross experiments that account for alternative hypotheses, we demonstrated amplified reproductive isolation specifically in the interspecific cross involving TE+ D. virilis, consistent with the action of dysgenesis-inducing TEs. These experiments demonstrate that TEs can contribute to hybrid incompatibilities via presence/absence polymorphisms.


2016 ◽  
Vol 6 (12) ◽  
pp. 4067-4076 ◽  
Author(s):  
Yasir H Ahmed-Braimah

Abstract Understanding the genetic basis of speciation is a central problem in evolutionary biology. Studies of reproductive isolation have provided several insights into the genetic causes of speciation, especially in taxa that lend themselves to detailed genetic scrutiny. Reproductive barriers have usually been divided into those that occur before zygote formation (prezygotic) and after (postzygotic), with the latter receiving a great deal of attention over several decades. Reproductive barriers that occur after mating but before zygote formation [postmating prezygotic (PMPZ)] are especially understudied at the genetic level. Here, I present a phenotypic and genetic analysis of a PMPZ reproductive barrier between two species of the Drosophila virilis group: D. americana and D. virilis. This species pair shows strong PMPZ isolation, especially when D. americana males mate with D. virilis females: ∼99% of eggs laid after these heterospecific copulations are not fertilized. Previous work has shown that the paternal loci contributing to this incompatibility reside on two chromosomes, one of which (chromosome 5) likely carries multiple factors. The other (chromosome 2) is fixed for a paracentric inversion that encompasses nearly half the chromosome. Here, I present two results. First, I show that PMPZ in this species cross is largely due to defective sperm storage in heterospecific copulations. Second, using advanced intercross and backcross mapping approaches, I identify genomic regions that carry genes capable of rescuing heterospecific fertilization. I conclude that paternal incompatibility between D. americana males and D. virilis females is underlain by four or more genes on chromosomes 2 and 5.


Genetics ◽  
1996 ◽  
Vol 143 (4) ◽  
pp. 1739-1752 ◽  
Author(s):  
Xavier Montagutelli ◽  
Rowena Turner ◽  
Joseph H Nadeau

Abstract Strong deviation of allele frequencies from Mendelian inheritance favoring Mus spretus-derived alleles has been described previously for X-linked loci in four mouse interspecific crosses. We reanalyzed data for three of these crosses focusing on the location of the gene(s) controlling deviation on the X chromosome and the genetic basis for incomplete deviation. At least two loci control deviation on the X chromosome, one near Xist (the candidate gene controlling X inactivation) and the other more centromerically located. In all three crosses, strong epistasis was found between loci near Xist and marker loci on the central portion of chromosome 2. The mechanism for this deviation from Mendelian expectations is not yet known but it is probably based on lethality of embryos carrying particular combinations of alleles rather than true segregation distortion during oogenesis in F1 hybrid females.


2020 ◽  
Vol 111 (5) ◽  
pp. 419-428 ◽  
Author(s):  
Marcella D Baiz ◽  
Priscilla K Tucker ◽  
Jacob L Mueller ◽  
Liliana Cortés-Ortiz

Abstract Reproductive isolation is a fundamental step in speciation. While sex chromosomes have been linked to reproductive isolation in many model systems, including hominids, genetic studies of the contribution of sex chromosome loci to speciation for natural populations are relatively sparse. Natural hybrid zones can help identify genomic regions contributing to reproductive isolation, like hybrid incompatibility loci, since these regions exhibit reduced introgression between parental species. Here, we use a primate hybrid zone (Alouatta palliata × Alouatta pigra) to test for reduced introgression of X-linked SNPs compared to autosomal SNPs. To identify X-linked sequence in A. palliata, we used a sex-biased mapping approach with whole-genome re-sequencing data. We then used genomic cline analysis with reduced-representation sequence data for parental A. palliata and A. pigra individuals and hybrids (n = 88) to identify regions with non-neutral introgression. We identified ~26 Mb of non-repetitive, putatively X-linked genomic sequence in A. palliata, most of which mapped collinearly to the marmoset and human X chromosomes. We found that X-linked SNPs had reduced introgression and an excess of ancestry from A. palliata as compared to autosomal SNPs. One outlier region with reduced introgression overlaps a previously described “desert” of archaic hominin ancestry on the human X chromosome. These results are consistent with a large role for the X chromosome in speciation across animal taxa and further, suggest shared features in the genomic basis of the evolution of reproductive isolation in primates.


2012 ◽  
Vol 2012 ◽  
pp. 1-11 ◽  
Author(s):  
Patrick M. Ferree ◽  
Satyaki Prasad

Satellites are one of the most enigmatic parts of the eukaryotic genome. These highly repetitive, noncoding sequences make up as much as half or more of the genomic content and are known to play essential roles in chromosome segregation during meiosis and mitosis, yet they evolve rapidly between closely related species. Research over the last several decades has revealed that satellite divergence can serve as a formidable reproductive barrier between sibling species. Here we highlight several key studies on Drosophila and other model organisms demonstrating deleterious effects of satellites and their rapid evolution on the structure and function of chromosomes in interspecies hybrids. These studies demonstrate that satellites can impact chromosomes at a number of different developmental stages and through distinct cellular mechanisms, including heterochromatin formation. These findings have important implications for how loci that cause postzygotic reproductive isolation are viewed.


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