scholarly journals Hybrid Sterility, Genetic Conflict and Complex Speciation: Lessons From the Drosophila simulans Clade Species

2021 ◽  
Vol 12 ◽  
Author(s):  
Daven C. Presgraves ◽  
Colin D. Meiklejohn
Keyword(s):  
Gene Flow ◽  
Male Sterility ◽  
Hybrid Sterility ◽  
Model Organism ◽  
Drosophila Simulans ◽  
Special Role ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Genetic Conflict ◽  
Modern Evolutionary Synthesis

The three fruitfly species of the Drosophila simulans clade— D. simulans, D. mauritiana, and D. sechellia— have served as important models in speciation genetics for over 40 years. These species are reproductively isolated by geography, ecology, sexual signals, postmating-prezygotic interactions, and postzygotic genetic incompatibilities. All pairwise crosses between these species conform to Haldane’s rule, producing fertile F1 hybrid females and sterile F1 hybrid males. The close phylogenetic proximity of the D. simulans clade species to the model organism, D. melanogaster, has empowered genetic analyses of their species differences, including reproductive incompatibilities. But perhaps no phenotype has been subject to more continuous and intensive genetic scrutiny than hybrid male sterility. Here we review the history, progress, and current state of our understanding of hybrid male sterility among the D. simulans clade species. Our aim is to integrate the available information from experimental and population genetics analyses bearing on the causes and consequences of hybrid male sterility. We highlight numerous conclusions that have emerged as well as issues that remain unresolved. We focus on the special role of sex chromosomes, the fine-scale genetic architecture of hybrid male sterility, and the history of gene flow between species. The biggest surprises to emerge from this work are that (i) genetic conflicts may be an important general force in the evolution of hybrid incompatibility, (ii) hybrid male sterility is polygenic with contributions of complex epistasis, and (iii) speciation, even among these geographically allopatric taxa, has involved the interplay of gene flow, negative selection, and positive selection. These three conclusions are marked departures from the classical views of speciation that emerged from the modern evolutionary synthesis.

scholarly journals The Genetics of Reproductive Isolation in the Drosophila simulans Clade: X vs. Autosomal Effects and Male vs. Female Effects

Genetics ◽  
1996 ◽  
Vol 143 (3) ◽  
pp. 1243-1255 ◽  
Author(s):  
Hope Hollocher ◽  
Chug-I Wu
Keyword(s):  
Reproductive Isolation ◽  
Male Sterility ◽  
X Chromosome ◽  
Hybrid Sterility ◽  
Drosophila Simulans ◽  
Female Sterility ◽  
Hybrid Male ◽  
Hybrid Female ◽  
Hybrid Male Sterility ◽  
Hybrid Inviability

Abstract A strong effect of homozygous autosomal regions on reproductive isolation was found for crosses between the species in the Drosophila simulans clade. Second chromosome regions were introgressed from D. mauritiana and D. sechellia into D. simulans and tested for their homozygous effects on hybrid male and hybrid female sterility and inviability. Most introgressions are fertile as heterozygotes, yet produce sterile male offspring when made homozygous. The density of homozygous autosomal factors contributing to hybrid male sterility is comparable to the density of X chromosome factors for this level of resolution. Female sterility was also revealed, yet the disparity between male and female levels of sterility was great, with male sterility being up to 23 times greater than female sterility. Complete hybrid inviability was also associated with some regions of the second chromosome, yet there were no strong sex differences. In conclusion, we find no evidence to support a strong X chromosome bias in the evolution of hybrid sterility or inviability but do find a very strong sex bias in the evolution of hybrid sterility. In light of these findings, we reevaluate the current models proposed to explain the genetic pattern of reproductive isolation.

scholarly journals The role of meiotic drive in hybrid male sterility

2010 ◽  
Vol 365 (1544) ◽  
pp. 1265-1272 ◽  
Author(s):  
Shannon R. McDermott ◽  
Mohamed A. F. Noor
Keyword(s):  
Male Sterility ◽  
Hybrid Sterility ◽  
Meiotic Drive ◽  
Mechanistic Explanation ◽  
Hybrid Progeny ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Species Formation ◽  
Allelic Segregation

Meiotic drive causes the distortion of allelic segregation away from Mendelian expected ratios, often also reducing fecundity and favouring the evolution of drive suppressors. If different species evolve distinct drive-suppressor systems, then hybrid progeny may be sterile as a result of negative interactions of these systems' components. Although the hypothesis that meiotic drive may contribute to hybrid sterility, and thus species formation, fell out of favour early in the 1990s, recent results showing an association between drive and sterility have resurrected this previously controversial idea. Here, we review the different forms of meiotic drive and their possible roles in speciation. We discuss the recent empirical evidence for a link between drive and hybrid male sterility, also suggesting a possible mechanistic explanation for this link in the context of chromatin remodelling. Finally, we revisit the population genetics of drive that allow it to contribute to speciation.

scholarly journals Extensive introgression despite Haldane’s rule: insights from grasshopper hybrid zones

2021 ◽  
Author(s):  
Linda Hagberg ◽  
Enrique Celemin ◽  
Iker Irisarri ◽  
Oliver Hawlitschek ◽  
J L Bella ◽  
...  
Keyword(s):  
Gene Flow ◽  
Reproductive Isolation ◽  
Male Sterility ◽  
Secondary Contact ◽  
Hybrid Zones ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
Species Formation

Although the process of species formation is notoriously idiosyncratic, the observation of pervasive patterns of reproductive isolation across species pairs suggests that generalities, or “rules”, underlie species formation in all animals. Haldane’s rule states that whenever a sex is absent, rare or sterile in a cross between two taxa, that sex is usually the heterogametic sex. Yet, understanding how Haldane’s rule first evolves and whether it is associated to genome wide barriers to gene flow remains a challenging task because this rule is usually studied in highly divergent taxa that no longer hybridize in nature. Here, we address these questions using the meadow grasshopper Pseudochorthippus parallelus where populations that readily hybridize in two natural hybrid zones show hybrid male sterility in laboratorial crosses. Using mitochondrial data, we infer that such populations have diverged some 100,000 years ago, surviving multiple glacial periods in isolated Pleistocenic refugia. Nuclear data shows that secondary contact has led to extensive introgression throughout the species range, including between populations showing hybrid male sterility. We find repeatable patterns of genomic differentiation across the two hybrid zones, yet such patterns are consistent with shared genomic constraints across taxa rather than their role in reproductive isolation. Together, our results suggest that Haldane’s rule can evolve relatively quickly within species, particularly when associated to strong demographic changes. At such early stages of species formation, hybrid male sterility still permits extensive gene flow, allowing future studies to identify genomic regions associated with reproductive barriers.

scholarly journals Mechanisms of transmission ratio distortion at hybrid sterility loci within and between Mimulus species

2017 ◽  
Author(s):  
Rachel E. Kerwin ◽  
Andrea L. Sweigart
Keyword(s):  
Male Sterility ◽  
Native Species ◽  
Hybrid Sterility ◽  
Transmission Ratio Distortion ◽  
Transmission Ratio ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Hybrid Incompatibility ◽  
Hybrid Transmission ◽  
Ratio Distortion

ABSTRACTHybrid incompatibilities are a common correlate of genomic divergence and a potentially important contributor to reproductive isolation. However, we do not yet have a detailed understanding of how hybrid incompatibility loci function and evolve within their native species, or why they are dysfunctional in hybrids. Here, we explore these issues for a well-studied, two-locus hybrid incompatibility between hybrid male sterility 1 (hms1) and hybrid male sterility 2 (hms2) in the closely related yellow monkeyflower species Mimulus guttatus and M. nasutus. By performing reciprocal backcrosses with introgression lines, we find evidence for gametic expression of the hms1-hms2 incompatibility. Surprisingly, however, hybrid transmission ratios at hms1 do not reflect this incompatibility, suggesting additional mechanisms counteract the effects of gametic sterility. Indeed, our backcross experiment shows hybrid transmission bias toward M. guttatus through both pollen and ovules, an effect that is particularly strong when hms2 is homozygous for M. nasutus alleles. In contrast, we find little evidence for hms1 transmission bias in crosses within M. guttatus, providing no indication of selfish evolution at this locus. Although we do not yet have sufficient genetic resolution to determine if hybrid sterility and transmission ratio distortion map to the same loci, our preliminary fine-mapping uncovers a genetically independent hybrid lethality system involving at least two loci linked to hms1. This fine-scale dissection of transmission ratio distortion at hms1 and hms2 provides insight into genomic differentiation between closely related Mimulus species and reveals multiple mechanisms of hybrid dysfunction.

scholarly journals Genetic Dissection of Hybrid Incompatibilities BetweenDrosophila simulansandD. mauritiana. I. Differential Accumulation of Hybrid Male Sterility Effects on theXand Autosomes

Genetics ◽  
2003 ◽  
Vol 164 (4) ◽  
pp. 1383-1398 ◽  
Author(s):  
Yun Tao ◽  
Sining Chen ◽  
Daniel L Hartl ◽  
Cathy C Laurie
Keyword(s):  
Male Sterility ◽  
X Chromosome ◽  
Rapid Evolution ◽  
Special Role ◽  
Genetic Dissection ◽  
Male Sterile ◽  
Hybrid Male ◽  
Evolutionary Mechanisms ◽  
Hybrid Male Sterility ◽  
Minimum Number

AbstractThe genetic basis of hybrid incompatibility in crosses between Drosophila mauritiana and D. simulans was investigated to gain insight into the evolutionary mechanisms of speciation. In this study, segments of the D. mauritiana third chromosome were introgressed into a D. simulans genetic background and tested as homozygotes for viability, male fertility, and female fertility. The entire third chromosome was covered with partially overlapping segments. Many segments were male sterile, while none were female sterile or lethal, confirming previous reports of the rapid evolution of hybrid male sterility (HMS). A statistical model was developed to quantify the HMS accumulation. In comparison with previous work on the X chromosome, we estimate that the X has ∼2.5 times the density of HMS factors as the autosomes. We also estimate that the whole genome contains ∼15 HMS “equivalents”—i.e., 15 times the minimum number of incompatibility factors necessary to cause complete sterility. Although some caveats for the quantitative estimate of a 2.5-fold density difference are described, this study supports the notion that the X chromosome plays a special role in the evolution of reproductive isolation. Possible mechanisms of a “large X” effect include selective fixation of new mutations that are recessive or partially recessive and the evolution of sex-ratio distortion systems.

scholarly journals Rampant Misexpression in a Mimulus (Monkeyflower) Introgression Line Caused by Hybrid Sterility, Not Regulatory Divergence

2020 ◽  
Vol 37 (7) ◽  
pp. 2084-2098 ◽  
Author(s):  
Rachel E Kerwin ◽  
Andrea L Sweigart
Keyword(s):  
Male Sterility ◽  
Gene Expression Regulation ◽  
Hybrid Sterility ◽  
Introgression Line ◽  
Transcript Abundance ◽  
Stabilizing Selection ◽  
Hybrid Male ◽  
Specific Expression ◽  
Hybrid Male Sterility ◽  
Genome Wide

Abstract Divergence in gene expression regulation is common between closely related species and may give rise to incompatibilities in their hybrid progeny. In this study, we investigated the relationship between regulatory evolution within species and reproductive isolation between species. We focused on a well-studied case of hybrid sterility between two closely related yellow monkeyflower species, Mimulus guttatus and Mimulus nasutus, that is caused by two epistatic loci, hybrid male sterility 1 (hms1) and hybrid male sterility 2 (hms2). We compared genome-wide transcript abundance across male and female reproductive tissues (i.e., stamens and carpels) from four genotypes: M. guttatus, M. nasutus, and sterile and fertile progeny from an advanced M. nasutus–M. guttatus introgression line carrying the hms1–hms2 incompatibility. We observed substantial variation in transcript abundance between M. guttatus and M. nasutus, including distinct but overlapping patterns of tissue-biased expression, providing evidence for regulatory divergence between these species. We also found rampant genome-wide misexpression, but only in the affected tissues (i.e., stamens) of sterile introgression hybrids carrying incompatible alleles at hms1 and hms2. Examining patterns of allele-specific expression in sterile and fertile introgression hybrids, we found evidence for interspecific divergence in cis- and trans-regulation, including compensatory cis–trans mutations likely to be driven by stabilizing selection. Nevertheless, species divergence in gene regulatory networks cannot explain the vast majority of the gene misexpression we observe in Mimulus introgression hybrids, which instead likely manifests as a downstream consequence of sterility itself.

Genetic analysis of hybrid sterility in crosses of the tsetse flies Glossina palpalis palpalis and Glossina palpalis gambiensis (Diptera: Glossinidae)

1997 ◽  
Vol 75 (7) ◽  
pp. 1109-1117 ◽  
Author(s):  
R. H. Gooding
Keyword(s):  
Linkage Group ◽  
Male Sterility ◽  
X Chromosome ◽  
Sex Chromosomes ◽  
Hybrid Sterility ◽  
Glossina Palpalis Palpalis ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Reciprocal Crosses ◽  
Glossina Palpalis

Reciprocal crosses of Glossina palpalis gambiensis Vanderplank and Glossina palpalis palpalis (Robineau-Desvoidy) were carried out using flies that had four marker genes on the X chromosome, two in linkage group II and one in linkage group III: The results of the reciprocal crosses conformed to Haldane's rule: F1 males were sterile and most F1 females were fertile. F1 females mated to G. p. gambiensis were more likely to be fertilized than females that were mated to G. p. palpalis. In three of the four experiments, the fertility of backcross females was not significantly different from that of F1 females, and there was little evidence that specific chromosomal combinations influenced the fertility of backcross females. Intrachromosomal recombination was lower in hybrid females than in G. p. palpalis. The major genetic factor associated with sterility among backcross males was the presence of sex chromosomes from two subspecies; a minor factor was the number of heterozygous autosomes, but interactions between sex chromosomes and autosomes from different taxa did not contribute to hybrid male sterility. Evidence is presented that a major factor causing hybrid male sterility lies between the loci tan (an eye color) and Est-t (testicular esterase) on the X chromosome. The use of differences between the fertility of males produced by backcrossing F1 females to the two parental subspecies as indicators that other X chromosome loci have a role in hybrid sterility is discussed.

scholarly journals Genetics of hybrid male sterility between drosophila sibling species: a complex web of epistasis is revealed in interspecific studies.

Genetics ◽  
1994 ◽  
Vol 138 (2) ◽  
pp. 329-341 ◽  
Author(s):  
M F Palopoli ◽  
C I Wu
Keyword(s):  
Male Sterility ◽  
X Chromosome ◽  
Functional Divergence ◽  
Hybrid Sterility ◽  
Sequence Divergence ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Common Component ◽  
Drosophila Mauritiana ◽  
Linkage Relationships

Abstract To study the genetic differences responsible for the sterility of their male hybrids, we introgressed small segments of an X chromosome from Drosophila simulans into a pure Drosophila mauritiana genetic background, then assessed the fertility of males carrying heterospecific introgressions of varying size. Although this analysis examined less than 20% of the X chromosome (roughly 5% of the euchromatic portion of the D. simulans genome), and the segments were introgressed in only one direction, a minimum of four factors that contribute to hybrid male sterility were revealed. At least two of the factors exhibited strong epistasis: males carrying either factor alone were consistently fertile, whereas males carrying both factors together were always sterile. Distinct spermatogenic phenotypes were observed for sterile introgressions of different lengths, and it appeared that an interaction between introgressed segments also influenced the stage of spermatogenic defect. Males with one category of introgression often produced large quantities of motile sperm and were observed copulating, but never inseminated females. Evidently these two species have diverged at a large number of loci which have varied effects on hybrid male fertility. By extrapolation, we estimate that there are at least 40 such loci on the X chromosome alone. Because these species exhibit little DNA-sequence divergence at arbitrarily chosen loci, it seems unlikely that the extensive functional divergence observed could be due mainly to random genetic drift. Significant epistasis between conspecific genes appears to be a common component of hybrid sterility between recently diverged species of Drosophila. The linkage relationships of interacting factors could shed light on the role played by epistatic selection in the dynamics of the allele substitutions responsible for reproductive barriers between species.

scholarly journals The genetic basis of Haldane's rule and the nature of asymmetric hybrid male sterility among Drosophila simulans, Drosophila mauritiana and Drosophila sechellia.

Genetics ◽  
1993 ◽  
Vol 134 (1) ◽  
pp. 251-260 ◽  
Author(s):  
L W Zeng ◽  
R S Singh
Keyword(s):  
Male Sterility ◽  
Y Chromosome ◽  
Genetic Basis ◽  
Drosophila Simulans ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Haldane’S Rule ◽  
Drosophila Sechellia ◽  
Haldane's Rule ◽  
Drosophila Mauritiana

Abstract Haldane's rule (i.e., the preferential hybrid sterility and inviability of heterogametic sex) has been known for 70 years, but its genetic basis, which is crucial to the understanding of the process of species formation, remains unclear. In the present study, we have investigated the genetic basis of hybrid male sterility using Drosophila simulans, Drosophila mauritiana and Drosophila sechellia. An introgression of D. sechellia Y chromosome into a fairly homogenous background of D. simulans did not show any effect of the introgressed Y on male sterility. The substitution of D. simulans Y chromosome into D. sechellia, and both reciprocal Y chromosome substitutions between D. simulans and D. mauritiana were unsuccessful. Introgressions of cytoplasm between D. simulans and D. mauritiana (or D. sechellia) also did not have any effect on hybrid male sterility. These results rule out the X-Y interaction hypothesis as a general explanation of Haldane's rule in this species group and indicate an involvement of an X-autosome interaction. Models of symmetrical and asymmetrical X-autosome interaction have been developed which explain the Y chromosome substitution results and suggest that evolution of interactions between different genetic elements in the early stages of speciation is more likely to be of an asymmetrical nature. The model of asymmetrical X-autosome interaction also predicts that different sets of interacting genes may be involved in different pairs of related species and can account for the observation that hybrid male sterility in many partially isolated species is often nonreciprocal or unidirectional.

Evidence for complex genic interactions between conspecific chromosomes underlying hybrid female sterility in the Drosophila simulans clade.

Genetics ◽  
1994 ◽  
Vol 137 (1) ◽  
pp. 191-199 ◽  
Author(s):  
A W Davis ◽  
E G Noonburg ◽  
C I Wu
Keyword(s):  
Hybrid Sterility ◽  
Drosophila Simulans ◽  
Female Sterility ◽  
Hybrid Male ◽  
Hybrid Female ◽  
Hybrid Male Sterility ◽  
Epistatic Interactions ◽  
X Chromosomes ◽  
F1 Hybrid ◽  
Drosophila Mauritiana

Abstract F1 hybrid females between the sibling species Drosophila simulans, Drosophila mauritiana and Drosophila sechellia are completely fertile. However, we have found that female sterility can be observed in F2 backcross females who are homozygous for D. simulans X chromosomes and homozygous for autosomal regions from either D. mauritiana or D. sechellia. Our results indicate that neither D. mauritiana autosome (2 or 3) can cause complete female sterility in a D. simulans background. The simultaneous presence of homozygous regions from both the second and third chromosomes of D. mauritiana, however, causes nearly complete female sterility which cannot be accounted for by their individual effects. The two autosomes of D. sechellia may show a similar pattern. From the same crosses, we also obtained evidence against a role for cytoplasmic or maternal effects in causing hybrid male sterility between these species. Taken with the results presented elsewhere, these observations suggest that epistatic interactions between conspecific genes in a hybrid background may be the prevalent mode of hybrid sterility between recently diverged species.

Sign in / Sign up

Export Citation Format

Share Document