A common suite of cellular abnormalities and spermatogenetic errors in sterile hybrid males in<i>Drosophila</i>

Kanippayoor, Rachelle L.; Alpern, Joshua H. M.; Moehring, Amanda J.

doi:10.1098/rspb.2019.2291

Cited by 8 publications

(14 citation statements)

References 71 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Here we present several lines of evidence implying that hybrid male sterility in Ficedula flycatchers is associated with a failure of meiosis and we propose candidate genes involved in genetic incompatibilities causing this failure. We conclude that dysfunctional meiosis most likely leads to aberrant chromosome segregation and/or faulty chromatin packing, similarly to what has been found in mouse (Mihola et al, 2009) and drosophila (Kanippayoor et al, 2020). This conclusion is based on combined evidence from whole genome DNA re-sequencing data, single cell transcriptomics of testis samples and testis histology sections.…”

Section: Discussionsupporting

confidence: 84%

The genomic basis of hybrid male sterility in Ficedula flycatchers

Marzal

Mugal

Cunha

et al. 2022

Preprint

View full text Add to dashboard Cite

Identifying genes involved in genetic incompatibilities causing hybrid sterility or inviability is a long-standing challenge in speciation research, especially in studies based on natural hybrid zones. Here we present the first high-probability candidate genes for hybrid male sterility in birds by using a combination of whole genome sequence data, histology sections of testis and single cell transcriptomics of testis samples from male pied-, collared-, and hybrid flycatchers. We reveal failure of meiosis in hybrid males and propose candidate genes involved in genetic incompatibilities causing this failure. Based on identification of genes with non-synonymous fixed differences between the two species and revealing miss-expression patterns of these genes across the various stages of hybrid male spermatogenesis we conclude aberrant chromosome segregation and/or faulty chromatin packing. A lower proportion of spermatids produced by hybrid males implies that a proportion of the aberrant spermatids undergo apoptosis. Finally, we report an overrepresentation of Z-linkage of the revealed candidate incompatibility genes. Our results challenge the assumption that speciation processes are driven by fast evolving genes by showing that a few changes in genes with highly conserved and central functions may quickly ensure reproductive isolation through post-zygotic isolation.

show abstract

Section: Discussionsupporting

confidence: 84%

The genomic basis of hybrid male sterility in Ficedula flycatchers

Marzal

Mugal

Cunha

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…In D. melanogaster , for example, the autosomal meiotic drive gene complex Segregation Distorter ( SD ) achieves a >95% transmission advantage from heterozygous SD/ + males by disrupting the histone-to-protamine transition for + -bearing spermatids that have large blocks of Rsp satDNA ( Wu et al, 1988 ; Gingell and McLean, 2020 ). In sterile F 1 hybrid males between D. simulans and D. mauritiana , sperm nuclei show an age-dependent de-condensation phenotype ( Kanippayoor et al, 2020 ), suggestive of compromised chromatin integrity, but whether specific misregulation of satDNAs is involved is unknown. [Spermatogenesis in sterile F 1 hybrid males from the reciprocal cross, in contrast, arrests during premeiotic stages ( Kulathinal and Singh, 1998 )].…”

Section: Sex Chromosomes and Hybrid Sterilitymentioning

confidence: 99%

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

Presgraves

Meiklejohn

2021

Front. Genet.

View full text Add to dashboard Cite

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.

show abstract

“…Since only heteromorphic sex chromosomes require this form of meiotic pairing, this mechanism could explain Haldane's rule. Chromosome separation failures during meiosis, leading to sterility in hybrids, have recently been reported for mice (Schwahn et al 2018) mosquitoes (Lang and Sharakhov 2019) yeast (Rogers et al 2018), and Drosophila (Kanippayoor et al 2020). Because haplodiploids lack sex chromosomes and males do not undergo meiosis to produce gametes, improper pairing of sex chromosomes cannot cause hybrid male sterility in haplodiploids, and hybrid males are therefore fertile.…”

Section: Discussionmentioning

confidence: 99%

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

Bendall

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

Evolutionary 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.

show abstract

A common suite of cellular abnormalities and spermatogenetic errors in sterile hybrid males inDrosophila

Cited by 8 publications

References 71 publications

The genomic basis of hybrid male sterility in Ficedula flycatchers

The genomic basis of hybrid male sterility in Ficedula flycatchers

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

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

Contact Info

Product

Resources

About