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

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.

Evolution ◽  
2005 ◽  
Vol 59 (5) ◽  
pp. 1016-1026 ◽  
Author(s):  
Michel Slotman ◽  
Alessandra Della Torre ◽  
Jeffrey R. Powell

Genetics ◽  
1995 ◽  
Vol 140 (1) ◽  
pp. 389-402 ◽  
Author(s):  
M Turelli ◽  
H A Orr

Abstract "HALDANE's rule" states that, if species hybrids of one sex only are inviable or sterile, the afflicted sex is much more likely to be heterogametic (XY) than homogametic (XX). We show that most or all of the phenomena associated with HALDANE's rule can be explained by the simple hypothesis that alleles decreasing hybrid fitness are partially recessive. Under this hypothesis, the XY sex suffers more than the XX because X-linked alleles causing postzygotic isolation tend to have greater cumulative effects when hemizygous than when heterozygous, even though the XX sex carries twice as many such alleles. The dominance hypothesis can also account for the "large X effect," the disproportionate effect of the X chromosome on hybrid inviability/sterility. In addition, the dominance theory is consistent with: the long temporal lag between the evolution of heterogametic and homogametic postzygotic isolation, the frequency of exceptions to HALDANE's rule, puzzling Drosophila experiments in which "unbalanced" hybrid females, who carry two X chromosomes from the same species, remain fertile whereas F1 hybrid males are sterile, and the absence of cases of HALDANE's rule for hybrid inviability in mammals. We discuss several novel predictions that could lead to rejection of the dominance theory.


2021 ◽  
Author(s):  
Neil Rosser ◽  
Nathaniel B. Edelman ◽  
Lucie Queste ◽  
Michaela Nelson ◽  
Fernando A. Seixas ◽  
...  

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.


Genetics ◽  
2000 ◽  
Vol 154 (4) ◽  
pp. 1663-1679 ◽  
Author(s):  
Michael Turelli ◽  
H Allen Orr

Abstract The sterility and inviability of species hybrids can be explained by between-locus “Dobzhansky-Muller” incompatibilities: alleles that are fit on their “normal” genetic backgrounds sometimes lower fitness when brought together in hybrids. We present a model of two-locus incompatibilities that distinguishes among three types of hybrid interactions: those between heterozygous loci (H0), those between a heterozygous and a homozygous (or hemizygous) locus (H1), and those between homozygous loci (H2). We predict the relative fitnesses of hybrid genotypes by calculating the expected numbers of each type of incompatibility. We use this model to study Haldane's rule and the large effect of X chromosomes on postzygotic isolation. We show that the severity of H0 vs. H1 incompatibilities is key to understanding Haldane's rule, while the severity of H1 vs. H2 incompatibilities must also be considered to explain large X effects. Large X effects are not inevitable in backcross analyses but rather—like Haldane's rule—may often reflect the recessivity of alleles causing postzygotic isolation. We also consider incompatibilities involving the Y (or W) chromosome and maternal effects. Such incompatibilities are common in Drosophila species crosses, and their consequences in male- vs. female-heterogametic taxa may explain the pattern of exceptions to Haldane's rule.


Evolution ◽  
2005 ◽  
Vol 59 (5) ◽  
pp. 1016 ◽  
Author(s):  
Michel Slotman ◽  
Alessandra della Torre ◽  
Jeffrey R. Powell

Genetics ◽  
2002 ◽  
Vol 161 (4) ◽  
pp. 1517-1526 ◽  
Author(s):  
Russell E Naisbit ◽  
Chris D Jiggins ◽  
Mauricio Linares ◽  
Camilo Salazar ◽  
James Mallet

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.


Genetics ◽  
1996 ◽  
Vol 143 (1) ◽  
pp. 603-607
Author(s):  
Ling-Wen Zeng

1968 ◽  
Vol 10 (2) ◽  
pp. 263-275 ◽  
Author(s):  
K. Lesins ◽  
A. Erac

In crosses between the two taxa Medicago striata Bast, and M. littoralis Rohde a high mortality of gametes and seedlings, and sterility of some plants were noted which were not related to gross chromosomal rearrangements. Although the F1, F2 and F3 generations from reciprocal crosses differed in chlorophyll deficiencies (indicating a cytoplasmic influence) a genic cause became evident from segregations for chlorophyll characters in the F2 and F3. Transference of the cytoplasmic factor by the pollen is indicative.Segregation for pod coiling direction indicated that the character was determined by one or two genetic factors of which the clockwise coiling direction is recessive. The spininess appeared to be determined by one genetic factor, of which the spineless allele is recessive.On the basis of genetic differences (especially on the built-in repulsion systems for normal chlorophyll development of opposite species) the two taxa should be considered two different species.


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