scholarly journals Complex basis of hybrid female sterility and Haldane's rule in Heliconius butterflies: Z-linkage and epistasis

2021 ◽  
Author(s):  
Neil Rosser ◽  
Nathaniel B. Edelman ◽  
Lucie Queste ◽  
Michaela Nelson ◽  
Fernando A. Seixas ◽  
...  
Keyword(s):  
Sex Chromosome ◽  
Hybrid Sterility ◽  
Differentially Expressed ◽  
F1 Hybrids ◽  
Female Sterility ◽  
Ovary Development ◽  
Z Chromosome ◽  
Hybrid Female ◽  
Haldane’S Rule ◽  
Haldane's Rule

Hybrids between diverging populations are often sterile or inviable. Hybrid unfitness usually evolves first in the heterogametic sex -- a pattern known as Haldane's rule. The genetics of Haldane's Rule have been extensively studied in species where the male is the heterogametic (XX/XY) sex, but its basis in taxa where the female is heterogametic (ZW/ZZ), such as Lepidoptera and birds, is largely unknown. Here, we analyse a new case of female hybrid sterility between geographic subspecies of Heliconius pardalinus. The two subspecies mate freely in captivity, but female F1 hybrids in both directions of cross are sterile. Sterility is due to arrested development of oocytes after they become differentiated from nurse cells, but before yolk deposition. We backcrossed fertile male F1 hybrids to parental females, and mapped quantitative trait loci (QTLs) for female sterility. We also identified genes differentially expressed in the ovary, and as a function of oocyte development. The Z chromosome has a major effect, similar to the "large X effect" in Drosophila, with strong epistatic interactions between loci at either end of the Z chromosome, and between the Z chromosome and autosomal loci on chromosomes 8 and 20. Among loci differentially expressed between females with arrested vs. non-arrested ovary development, we identified six candidate genes known also from Drosophila melanogaster and Parage aegeria oogenesis. This study is the first to characterize hybrid sterility using genome mapping in the Lepidoptera. We demonstrate that sterility is produced by multiple complex epistastic interactions often involving the sex chromosome, as predicted by the dominance theory of Haldane's Rule.

scholarly journals Hybrid Sterility, Haldane's Rule and Speciation in Heliconius cydno and H. melpomene

Genetics ◽  
2002 ◽  
Vol 161 (4) ◽  
pp. 1517-1526 ◽  
Author(s):  
Russell E Naisbit ◽  
Chris D Jiggins ◽  
Mauricio Linares ◽  
Camilo Salazar ◽  
James Mallet
Keyword(s):  
Hybrid Sterility ◽  
Female Offspring ◽  
F1 Hybrids ◽  
Female Sterility ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
In The Wild ◽  
Multiple Routes ◽  
Female Hybrid ◽  
Heterogametic Sex

Abstract Most genetic studies of Haldane's rule, in which hybrid sterility or inviability affects the heterogametic sex preferentially, have focused on Drosophila. It therefore remains unclear to what extent the conclusions of that work apply more generally, particularly in female-heterogametic taxa such as birds and Lepidoptera. Here we present a genetic analysis of Haldane's rule in Heliconius butterflies. Female F1 hybrids between Heliconius melpomene and H. cydno are completely sterile, while males have normal to mildly reduced fertility. In backcrosses of male F1 hybrids, female offspring range from completely sterile to fully fertile. Linkage analysis using the Z-linked triose-phosphate isomerase locus demonstrates a “large X” (Z) effect on sterility. Expression of female sterility varies among crosses in this and a previous study of Heliconius. Sterility may result from the production of normal but infertile eggs, production of small infertile eggs, or from a complete failure to develop ovarioles, which suggests multiple routes to the evolution of hybrid sterility in these Heliconius species. These results conform to the expectations of the “dominance” rather than “faster male” theories of Haldane's rule and suggest that relatively few loci are responsible. The two species are broadly sympatric and hybridize in the wild, so that female hybrid sterility forms one of several strong but incomplete barriers to gene flow in nature. The effect of female sterility is comparable to that of selection against non-mimetic hybrids, while mate choice forms a much stronger barrier to gene transfer.

scholarly journals Complex basis of hybrid female sterility and Haldane’s rule in Heliconius butterflies: Z‐linkage and epistasis

2021 ◽  
Author(s):  
Neil Rosser ◽  
Nathaniel B. Edelman ◽  
Lucie M. Queste ◽  
Michaela Nelson ◽  
Fernando Seixas ◽  
...  
Keyword(s):  
Female Sterility ◽  
Hybrid Female ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
Heliconius Butterflies ◽  
Complex Basis

SEX CHROMOSOME TRANSLOCATIONS IN THE EVOLUTION OF REPRODUCTIVE ISOLATION

Genetics ◽  
1972 ◽  
Vol 72 (2) ◽  
pp. 317-333
Author(s):  
Martin L Tracey
Keyword(s):  
Reproductive Isolation ◽  
X Chromosome ◽  
Sex Chromosome ◽  
Hybrid Sterility ◽  
Fixation Probability ◽  
Chromosomal Imbalance ◽  
Haldane’S Rule ◽  
Chromosome Translocations ◽  
Haldane's Rule ◽  
Heterogametic Sex

ABSTRACT Haldane's rule states that in organisms with differentiated sex chromosomes, hybrid sterility or inviability is generally expressed more frequently in the heterogametic sex. This observation has been variously explained as due to either genic or chromosomal imbalance. The fixation probabilities and mean times to fixation of sex-chromosome translocations of the type necessary to explain Haldane's rule on the basis of chromosomal imbalance have been estimated in small populations of Drosophila melanogaster. The fixation probability of an X chromosome carrying the long arm of the Y(X.YL) is approximately 30% greater than expected under the assumption of no selection. No fitness differences associated with the attached YL segment were detected. The fixation probability of a deficient Y chromosome is 300% greater than expected when the X chromosome contains the deleted portion of the Y. It is suggested that sex-chromosome translocations may play a role in the establishment of reproductive isolation.

scholarly journals FEMALE STERILITY IN HYBRIDS BETWEEN ANOPHELES GAMBIAE AND A. ARABIENSIS, AND THE CAUSES OF HALDANE'S RULE

Evolution ◽  
2005 ◽  
Vol 59 (5) ◽  
pp. 1016-1026 ◽  
Author(s):  
Michel Slotman ◽  
Alessandra Della Torre ◽  
Jeffrey R. Powell
Keyword(s):  
Anopheles Gambiae ◽  
Female Sterility ◽  
Haldane’S Rule ◽  
Haldane's Rule

scholarly journals Asymmetric Phenotypes of Sterile Hybrid Males From Reciprocal Crosses Between Species of the Anopheles gambiae Complex

2021 ◽  
Vol 9 ◽  
Author(s):  
Jiangtao Liang ◽  
James M. Hodge ◽  
Igor V. Sharakhov
Keyword(s):  
Anopheles Gambiae ◽  
Molecular Mechanisms ◽  
Genetic Factors ◽  
F1 Hybrids ◽  
Sterile Hybrid ◽  
Reciprocal Crosses ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
Normal Period ◽  
Species Hybrids

Haldane’s rule of speciation states that sterility or inviability affects the heterogametic sex of inter-species hybrids. Darwin’s corollary to Haldane’s rule implies that there are asymmetric phenotypes in inter-species hybrids from reciprocal crosses. Studying the phenotypes of F1 hybrids among closely related species of malaria mosquitoes can assist researchers in identifying the genetic factors and molecular mechanisms of speciation. To characterize phenotypes of sterile hybrid males in the Anopheles gambiae complex, we performed crosses between laboratory strains of An. merus and either An. gambiae or An. coluzzii. The reproductive tracts had normal external morphology in hybrid males from crosses between female An. merus and male An. gambiae or An. coluzzii. Despite being sterile, these males could copulate with females for a normal period of time and could transfer a mating plug to induce female oviposition and monogamy. In contrast, the entire reproductive tracts in hybrid males from crosses between female An. gambiae or An. coluzzii and male An. merus were severely underdeveloped. These males had atrophic testes and reduced somatic organs of the reproductive system including male accessary glands and ejaculatory duct. In addition, hybrid males with underdeveloped reproductive tracts displayed a shorter copulation time with females and failed to induce female oviposition and monogamy due to their inability to form and transfer a plug to females during mating. The asymmetry of the phenotypes associated with hybrid male sterility suggests that different genetic factors and molecular mechanisms are responsible for reproductive isolation in reciprocal crosses among species of the An. gambiae complex.

scholarly journals The avian W chromosome is a refugium for endogenous retroviruses with likely effects on female-biased mutational load and genetic incompatibilities

2021 ◽  
Vol 376 (1833) ◽  
pp. 20200186
Author(s):  
Valentina Peona ◽  
Octavio M. Palacios-Gimenez ◽  
Julie Blommaert ◽  
Jing Liu ◽  
Tri Haryoko ◽  
...  
Keyword(s):  
Sex Chromosome ◽  
Gene Dosage ◽  
Endogenous Retroviruses ◽  
Mass Spectrometry Data ◽  
Mutational Load ◽  
W Chromosome ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
Genome Wide ◽  
Female Specific

It is a broadly observed pattern that the non-recombining regions of sex-limited chromosomes (Y and W) accumulate more repeats than the rest of the genome, even in species like birds with a low genome-wide repeat content. Here, we show that in birds with highly heteromorphic sex chromosomes, the W chromosome has a transposable element (TE) density of greater than 55% compared to the genome-wide density of less than 10%, and contains over half of all full-length (thus potentially active) endogenous retroviruses (ERVs) of the entire genome. Using RNA-seq and protein mass spectrometry data, we were able to detect signatures of female-specific ERV expression. We hypothesize that the avian W chromosome acts as a refugium for active ERVs, probably leading to female-biased mutational load that may influence female physiology similar to the ‘toxic-Y’ effect in Drosophila males. Furthermore, Haldane's rule predicts that the heterogametic sex has reduced fertility in hybrids. We propose that the excess of W-linked active ERVs over the rest of the genome may be an additional explanatory variable for Haldane's rule, with consequences for genetic incompatibilities between species through TE/repressor mismatches in hybrids. Together, our results suggest that the sequence content of female-specific W chromosomes can have effects far beyond sex determination and gene dosage. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.

scholarly journals Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane's rule and related phenomena.

Genetics ◽  
1991 ◽  
Vol 128 (4) ◽  
pp. 841-858 ◽  
Author(s):  
L D Hurst ◽  
A Pomiankowski
Keyword(s):  
Sex Ratio ◽  
Sex Chromosome ◽  
Meiotic Drive ◽  
Maternal Transmission ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
Sex Ratio Bias ◽  
Y Chromosomes ◽  
Heterogametic Sex ◽  
Hybrid Cross

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.

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