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

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 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

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

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

Genetic Complexity Underlying Hybrid Male Sterility in Drosophila

Genetics ◽  
2004 ◽  
Vol 166 (2) ◽  
pp. 789-796 ◽  
Author(s):  
Kyoichi Sawamura ◽  
John Roote ◽  
Chung-I Wu ◽  
Masa-Toshi Yamamoto
Keyword(s):  
Male Sterility ◽  
Related Species ◽  
Synergistic Effects ◽  
Female Sterility ◽  
Hybrid Male ◽  
Hybrid Female ◽  
Hybrid Male Sterility ◽  
Closely Related Species ◽  
Genetic Complexity ◽  
Recessive Genes

Abstract Recent genetic analyses of closely related species of Drosophila have indicated that hybrid male sterility is the consequence of highly complex synergistic effects among multiple genes, both conspecific and heterospecific. On the contrary, much evidence suggests the presence of major genes causing hybrid female sterility and inviability in the less-related species, D. melanogaster and D. simulans. Does this contrast reflect the genetic distance between species? Or, generally, is the genetic basis of hybrid male sterility more complex than that of hybrid female sterility and inviability? To clarify this point, the D. simulans introgression of the cytological region 34D-36A to the D. melanogaster genome, which causes recessive male sterility, was dissected by recombination, deficiency, and complementation mapping. The 450-kb region between two genes, Suppressor of Hairless and snail, exhibited a strong effect on the sterility. Males are (semi-)sterile if this region of the introgression is made homozygous or hemizygous. But no genes in the region singly cause the sterility; this region has at least two genes, which in combination result in male sterility. Further, the males are less fertile when heterozygous with a larger introgression, which suggests that dominant modifiers enhance the effects of recessive genes of male sterility. Such an epistatic view, even in the less-related species, suggests that the genetic complexity is special to hybrid male sterility.

scholarly journals Resurrecting Muller's Theory of Haldane's Rule

Genetics ◽  
1996 ◽  
Vol 143 (1) ◽  
pp. 603-607
Author(s):  
Ling-Wen Zeng
Keyword(s):  
Haldane’S Rule ◽  
Haldane's Rule

A Novel System of Fertility Rescue in Drosophila Hybrids Reveals a Link Between Hybrid Lethality and Female Sterility

Genetics ◽  
2003 ◽  
Vol 163 (1) ◽  
pp. 217-226 ◽  
Author(s):  
Daniel A Barbash ◽  
Michael Ashburner
Keyword(s):  
Drosophila Melanogaster ◽  
Low Temperature ◽  
Genetic Basis ◽  
Female Sterility ◽  
Hybrid Lethality ◽  
Hybrid Male ◽  
Hybrid Female ◽  
F1 Hybrid ◽  
Drosophila Gene

Abstract Hybrid daughters of crosses between Drosophila melanogaster females and males from the D. simulans species clade are fully viable at low temperature but have agametic ovaries and are thus sterile. We report here that mutations in the D. melanogaster gene Hybrid male rescue (Hmr), along with unidentified polymorphic factors, rescue this agametic phenotype in both D. melanogaster/D. simulans and D. melanogaster/D. mauritiana F1 female hybrids. These hybrids produced small numbers of progeny in backcrosses, their low fecundity being caused by incomplete rescue of oogenesis as well as by zygotic lethality. F1 hybrid males from these crosses remained fully sterile. Hmr+ is the first Drosophila gene shown to cause hybrid female sterility. These results also suggest that, while there is some common genetic basis to hybrid lethality and female sterility in D. melanogaster, hybrid females are more sensitive to fertility defects than to lethality.

scholarly journals Differences in offspring size predict the direction of isolation asymmetry between populations of a placental fish

2013 ◽  
Vol 9 (5) ◽  
pp. 20130327 ◽  
Author(s):  
Matthew Schrader ◽  
Rebecca C. Fuller ◽  
Joseph Travis
Keyword(s):  
Reproductive Isolation ◽  
Offspring Size ◽  
Hybrid Inviability ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
Asymmetric Pattern ◽  
Heterandria Formosa ◽  
Different Populations ◽  
Selection For

Crosses between populations or species often display an asymmetry in the fitness of reciprocal F 1 hybrids. This pattern, referred to as isolation asymmetry or Darwin's Corollary to Haldane's Rule, has been observed in taxa from plants to vertebrates, yet we still know little about which factors determine its magnitude and direction. Here, we show that differences in offspring size predict the direction of isolation asymmetry observed in crosses between populations of a placental fish, Heterandria formosa . In crosses between populations with differences in offspring size, high rates of hybrid inviability occur only when the mother is from a population characterized by small offspring. Crosses between populations that display similarly sized offspring, whether large or small, do not result in high levels of hybrid inviability in either direction. We suggest this asymmetric pattern of reproductive isolation is due to a disruption of parent–offspring coadaptation that emerges from selection for differently sized offspring in different populations.

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