scholarly journals Lack of intrinsic postzygotic isolation in haplodiploid male hybrids despite high genetic distance

2020 ◽  
Author(s):  
Emily E. Bendall ◽  
Kayla M. Mattingly ◽  
Amanda J. Moehring ◽  
Catherine R. Linnen

AbstractEvolutionary biologists have long been interested in understanding the mechanisms underlying Haldane’s rule. The explanatory theories of dominance and faster-X, which are based on recessive alleles being expressed in the heterogametic sex, have been proposed as common mechanisms. These mechanisms predict that greater hemizygosity leads to both faster evolution and greater expression of intrinsic postzygotic isolation. Under these mechanisms, haplodiploids should evolve and express intrinsic postzygotic isolation faster than diploids because the entire genome is analogous to a sex chromosome. Here, we measure sterility and inviability in hybrids between Neodiprion pinetum and N. lecontei, a pair of haplodiplopids that differ morphologically, behaviorally, and genetically. We compare the observed isolation to that expected from published estimates of isolation in diploids at comparable levels of genetic divergence. We find that both male and female hybrids are viable and fertile, which is less isolation than expected. We then discuss several potential explanations for this surprising lack of isolation, including alternative mechanisms for Haldane’s rule and a frequently overlooked quirk of haplodiploid genetics that may slow the emergence of complete intrinsic postzygotic isolation in hybrid males. Finally, we describe how haplodiploids, an underutilized resource, can be used to differentiate between mechanisms of Haldane’s rule.

Genetics ◽  
1991 ◽  
Vol 128 (4) ◽  
pp. 841-858 ◽  
Author(s):  
L D Hurst ◽  
A Pomiankowski

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.


Genetics ◽  
1972 ◽  
Vol 72 (2) ◽  
pp. 317-333
Author(s):  
Martin L Tracey

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.


2021 ◽  
Author(s):  
Janne Swaegers ◽  
Rosa Ana Sanchez-Guillen ◽  
Pallavi Chauhan ◽  
Maren Wellenreuther ◽  
Bengt Hansson

Contemporary hybrid zones act as natural laboratories for the investigation of species boundaries and allow to shed light on the little understood roles of sex chromosomes in species divergence. Sex chromosomes are considered to function as a hotspot of genetic divergence between species; indicated by less genomic introgression compared to autosomes during hybridisation. Moreover, they are thought to contribute to Haldane's rule which states that hybrids of the heterogametic sex are more likely to be inviable or sterile. To test these hypotheses, we used contemporary hybrid zones of Ischnura elegans, a damselfly species that has been expanding its range into the northern and western regions of Spain, leading to chronic hybridization with its sister species Ischnura graellsii. We analysed genome-wide SNPs in the Spanish I. elegans and I. graellsii hybrid zone and found (i) that the X chromosome shows less genomic introgression compared to autosomes and (ii) that males are underrepresented among admixed individuals as predicted by Haldane's rule. This is the first study in Odonata that suggests a role of the X chromosome in reproductive isolation. Moreover, our data adds to the few studies on species with X0 sex determination system and contradicts the hypothesis that the absence of a Y chromosome causes exceptions to Haldane's rule.


2020 ◽  
Vol 16 (3) ◽  
pp. 20190867 ◽  
Author(s):  
Zoe A. Xirocostas ◽  
Susan E. Everingham ◽  
Angela T. Moles

Many taxa show substantial differences in lifespan between the sexes. However, these differences are not always in the same direction. In mammals, females tend to live longer than males, while in birds, males tend to live longer than females. One possible explanation for these differences in lifespan is the unguarded X hypothesis, which suggests that the reduced or absent chromosome in the heterogametic sex (e.g. the Y chromosome in mammals and the W chromosome in birds) exposes recessive deleterious mutations on the other sex chromosome. While the unguarded X hypothesis is intuitively appealing, it had never been subject to a broad test. We compiled male and female longevity data for 229 species spanning 99 families, 38 orders and eight classes across the tree of life. Consistent with the unguarded X hypothesis, a meta-analysis showed that the homogametic sex, on average, lives 17.6% longer than the heterogametic sex. Surprisingly, we found substantial differences in lifespan dimorphism between female heterogametic species (in which the homogametic sex lives 7.1% longer) and male heterogametic species (in which the homogametic sex lives 20.9% longer). Our findings demonstrate the importance of considering chromosome morphology in addition to sexual selection and environment as potential drivers of sexual dimorphism, and advance our fundamental understanding of the mechanisms that shape an organism's lifespan.


2020 ◽  
Vol 287 (1928) ◽  
pp. 20200690 ◽  
Author(s):  
Richard Allen ◽  
Hannah Ryan ◽  
Brian W. Davis ◽  
Charlotte King ◽  
Laurent Frantz ◽  
...  

Numerous pairs of evolutionarily divergent mammalian species have been shown to produce hybrid offspring. In some cases, F 1 hybrids are able to produce F 2 s through matings with F 1 s. In other instances, the hybrids are only able to produce offspring themselves through backcrosses with a parent species owing to unisexual sterility (Haldane's Rule). Here, we explicitly tested whether genetic distance, computed from mitochondrial and nuclear genes, can be used as a proxy to predict the relative fertility of the hybrid offspring resulting from matings between species of terrestrial mammals. We assessed the proxy's predictive power using a well-characterized felid hybrid system, and applied it to modern and ancient hominins. Our results revealed a small overlap in mitochondrial genetic distance values that distinguish species pairs whose calculated distances fall within two categories: those whose hybrid offspring follow Haldane's Rule, and those whose hybrid F 1 offspring can produce F 2 s. The strong correlation between genetic distance and hybrid fertility demonstrated here suggests that this proxy can be employed to predict whether the hybrid offspring of two mammalian species will follow Haldane's Rule.


The Auk ◽  
2000 ◽  
Vol 117 (3) ◽  
pp. 578-585 ◽  
Author(s):  
Catherine E. Smith ◽  
Sievert Rohwer

Abstract We introduce a phenotypic method to test for excess mortality in hybrids of the heterogametic sex, as expected from Haldane's rule, and apply this method to the unusually narrow hybrid zones between Hermit Warblers (Dendroica occidentalis) and Townsend's Warblers (D. townsendi) in the Pacific Northwest. Our test requires establishing comparable hybrid indices for male and female warblers. The hybrid index that we developed for females produced age-corrected distributions for phenotypically pure reference samples that closely matched those used by Rohwer and Wood (1998) for males. The similarity in these distributions enabled us to compare the relative frequency of males and females in hybrids and parentals. We detected no deficiency of hybrid females and thus no inviability in the heterogametic sex. Our failure to find evidence of the inviability component of Haldane's rule is not unexpected given the close relationship between these taxa; nonetheless, our methods should be generally useful for studies of hybrid zones.


2019 ◽  
Vol 4 (1) ◽  
Author(s):  
Mohsen A. Ahmed ◽  
Yousif M.S. Al-Barzinji ◽  
Lanja Assad Ismail

The objective of the present study was to determine genetic diversity among three geese color types using RAPD markers and hematological parameters. The overall mean, of the live weights, Hemoglobin, Hetrophil %, Lymphocyte %, Monocyte %, and H/L ratio were 3.006 (kg), 14.64, 36.896, 49.896, 2.233 and 0.736 respectively. The breed, sex and interaction between them have a significant effect on live body weight, Hemoglobin, and Monocyte %. Ten primers were used and six out of them were selected based on their number of bands (NB) and polymorphic characteristics. A total of 309 bands observed, ranged from 30 in primer OPB-07 to 54 bands in OPA-20. Five unique bands were found only in white goose, whereas the highest unique band was obtained in primer OPB-01 locus. Overall genetic distance among native geese arrived 64.122 and phylogenetic dendrograms showed that 3 clusters, the first cluster content only white geese (Male and Female) breed, the second one cluster is included piebald geese breed (Male and female) and the third one was including gray geese (Male and female) breed. It was concluded that the white geese was closer to piebald geese than to the gray geese breed. The high genetic distance (64.122%) and variation in phenotypic value such as live weight (2.375 to 3.600 kg/bird) for three native geese indicate that these native geese have a good amount of genetic resources to made genetically improvement in further and it means the three goose samples are independent breeds. 


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.


Genetics ◽  
1994 ◽  
Vol 138 (3) ◽  
pp. 791-799
Author(s):  
M J Wade ◽  
N A Johnson ◽  
G Wardle

Abstract Haldane's rule states that, in interspecific crosses, when hybrid viability or fertility is diminished more in one sex of the hybrids than in the other, the heterogametic sex is more adversely affected. We used quantitative genetic methods to investigate the genetic basis of variation for the expression of the viability aspect of Haldane's rule when Tribolium castaneum males are crossed to Tribolium freemani females. Using a half-sib design, we found significant genetic variance for the expression of Haldane's rule, i.e., variation among T. castaneum sires in the hybrid sex ratios produced by their sons. We also derived 23 independent lineages from the same base population by 8 generations of brother-sister mating. From the same experiments, we also found heritable variation among surviving hybrid males in the incidence of antennal deformities. Upon inbreeding, the variance of both traits (hybrid sex ratio and proportion deformities) increased substantially but the means changed little. Because fitness within T. castaneum lineages declined substantially with inbreeding, we infer that hybrid male viability may have a different genetic basis than viability fitness within species. Deleterious recessive alleles held within species by mutation/selection balance appear not to be a major contributor to hybrid incompatibility.


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