Chromosomal rearrangements in holocentric organisms lead to reproductive isolation by hybrid dysfunction: The correlation between karyotype rearrangements and germination rates in sedges

Abstract In evolutionarily young species and sympatric host races of phytophagous insects, postzygotic incompatibility is often not yet fully developed, but reduced fitness of hybrids is thought to facilitate further divergence. However, empirical evidence supporting this hypothesis is limited. To assess the role of reduced hybrid fitness, we studied meiosis and fertility in hybrids of two closely related small ermine moths, Yponomeuta padella and Yponomeuta cagnagella, and determined the extent of intrinsic postzygotic reproductive isolation. We found extensive rearrangements between the karyotypes of the two species and irregularities in meiotic chromosome pairing in their hybrids. The fertility of reciprocal F1 and, surprisingly, also of backcrosses with both parental species was not significantly decreased compared with intraspecific offspring. The results indicate that intrinsic postzygotic reproductive isolation between these closely related species is limited. We conclude that the observed chromosomal rearrangements are probably not the result of an accumulation of postzygotic incompatibilities preventing hybridization. Alternative explanations, such as adaptation to new host plants, are discussed.

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Centromere scission drives chromosome shuffling and reproductive isolation

10.1101/809848 ◽

2019 ◽

Cited By ~ 1

Author(s):

Vikas Yadav ◽

Sheng Sun ◽

Marco A. Coelho ◽

Joseph Heitman

Keyword(s):

Reproductive Isolation ◽

Sexual Reproduction ◽

Large Scale ◽

Chromosomal Rearrangements ◽

Genome Structure ◽

Chromosome Translocation ◽

Dna Double Strand Breaks ◽

Chromosome Translocations ◽

Genomic Studies ◽

Eukaryotic Organisms

AbstractA fundamental characteristic of eukaryotic organisms is the generation of genetic variation via sexual reproduction. Conversely, significant large-scale genome structure variations could hamper sexual reproduction, causing reproductive isolation and promote speciation. The underlying processes behind large-scale genome rearrangements are not well understood and include chromosome translocations involving centromeres. Recent genomic studies in the Cryptococcus species complex revealed that chromosome translocations generated via centromere recombination have reshaped the genomes of different species. In this study, multiple DNA double-strand breaks (DSBs) were generated via the CRISPR/Cas9 system at centromere-specific retrotransposons in the human fungal pathogen Cryptococcus neoformans. The resulting DSBs were repaired in a complex manner, leading to the formation of multiple inter-chromosomal rearrangements and new telomeres, similar to chromothripsis-like events. The newly generated strains harboring chromosome translocations exhibited normal vegetative growth but failed to undergo successful sexual reproduction with the parental wild-type strain. One of these strains failed to produce any spores, while another produced ∼3% viable progeny. The germinated progeny exhibited aneuploidy for multiple chromosomes and showed improved fertility with both parents. All chromosome translocation events were accompanied without any detectable change in gene sequences and thus, suggest that chromosomal translocations alone may play an underappreciated role in the onset of reproductive isolation and speciation.

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Speciation and the developmental alarm clock

10.1101/2020.07.08.193698 ◽

2020 ◽

Author(s):

Asher D. Cutter ◽

Joanna D. Bundus

Keyword(s):

New Species ◽

Molecular Evolution ◽

Reproductive Isolation ◽

Molecular Mechanisms ◽

Developmental Stages ◽

Genetic Network ◽

Alarm Clock ◽

Developmental System Drift ◽

Evo Devo ◽

Hybrid Dysfunction

AbstractNew species arise as the genomes of populations diverge. The developmental ‘alarm clock’ of speciation sounds off when sufficient divergence in genetic control of development leads hybrid individuals to infertility or inviability, the world awoken to the dawn of new species with intrinsic post-zygotic reproductive isolation. Some developmental stages will be more prone to hybrid dysfunction due to how molecular evolution interacts with the ontogenetic timing of gene expression. Considering the ontogeny of hybrid incompatibilities provides a profitable connection between ‘evo-devo’ and speciation genetics to better link macroevolutionary pattern, microevolutionary process, and molecular mechanisms. Here we explore speciation alongside development, emphasizing their mutual dependence on genetic network features, fitness landscapes, and developmental system drift. We assess models for how ontogenetic timing of reproductive isolation can be predictable. Experiments and theory within this synthetic perspective can help identify new rules of speciation as well as rules in the molecular evolution of development.Impact StatementIntegrating speciation genetics with ontogeny can identify predictable rules in the molecular evolution of developmental pathways and in the accumulation of reproductive isolation as genomes diverge.

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Estimating the genic and chromosomal components of reproductive isolation within and between subspecies of the grasshopper Caledia captiva

Canadian Journal of Genetics and Cytology ◽

10.1139/g86-098 ◽

1986 ◽

Vol 28 (5) ◽

pp. 686-695 ◽

Cited By ~ 12

Author(s):

D. D. Shaw ◽

D. J. Coates ◽

P. Wilkinson

Keyword(s):

Reproductive Isolation ◽

Hybrid Zone ◽

Chromosomal Rearrangements ◽

End Points ◽

Experimental Hybridization ◽

Repeat Dna ◽

Dna Profiles ◽

Southeast Queensland

Previous studies have indicated that the Moreton and Torresian subspecies of the grasshopper Caledia captiva are distinguished by a series of pericentric rearrangements involving 8 of the 12 members of the genome. In addition, they show distinctive allozyme patterns with[Formula: see text]. The two taxa meet in southeast Queensland where they form a narrow hybrid zone. Experimental hybridization between the taxa reveals that the F2 generation is totally inviable and backcrosses are 53–64% inviable.A major component of inviability is correlated with the redistribution of chiasmata which occurs in F1 heterozygotes and leads to the production of novel recombinant chromosomes. However, the relative contributions of the effects of chromosomal heterozygosity versus those effects because of genic divergence could not be distinguished. The discovery that the metacentric Moreton subspecies represents the northerly limit of a continuous chromosomal cline has resolved this problem. At the southern end of the cline (Lakes Entrance), the karyotype is composed entirely of acro- and telo-centric chromosomes which are equivalent in their gross structure to the Torresian karyotype and there is no redistribution of chiasmata in (LE × TT) F1 hybrids. However, the Lakes Entrance population still retains allozymic and highly repeat DNA profiles similar to the Moreton taxon. Crosses between Moreton and Lakes Entrance, which are genically equivalent but chromosomally divergent, show 42% inviability in the F2 generation. Similarly, when the chromosomal component is removed, as in the (LE × TT) cross, F2 and backcross viabilities are improved by 46 and 21–36%, respectively.These data clearly indicate that the pericentric rearrangements which distinguish both the end points of the continuous cline and the two parapatric subspecies are involved in postmating reproductive isolation.Key words: chromosomal rearrangements, reproductive isolation, speciation, clines.

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Reproductive isolation in a nascent species pair is associated with aneuploidy in hybrid offspring

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2014.2862 ◽

2015 ◽

Vol 282 (1802) ◽

pp. 20142862 ◽

Cited By ~ 19

Author(s):

Anne-Marie Dion-Côté ◽

Radka Symonová ◽

Petr Ráb ◽

Louis Bernatchez

Keyword(s):

Reproductive Isolation ◽

Chromosome Numbers ◽

Chromosomal Instability ◽

Diploid Number ◽

Chromosomal Rearrangements ◽

Coregonus Clupeaformis ◽

Lake Whitefish ◽

Mitotic Instability ◽

Two Populations

Speciation may occur when the genomes of two populations accumulate genetic incompatibilities and/or chromosomal rearrangements that prevent inter-breeding in nature. Chromosome stability is critical for survival and faithful transmission of the genome, and hybridization can compromise this. However, the role of chromosomal stability on hybrid incompatibilities has rarely been tested in recently diverged populations. Here, we test for chromosomal instability in hybrids between nascent species, the ‘dwarf’ and ‘normal’ lake whitefish ( Coregonus clupeaformis ). We examined chromosomes in pure embryos, and healthy and malformed backcross embryos. While pure individuals displayed chromosome numbers corresponding to the expected diploid number (2 n = 80), healthy backcrosses showed evidence of mitotic instability through an increased variance of chromosome numbers within an individual. In malformed backcrosses, extensive aneuploidy corresponding to multiples of the haploid number (1 n = 40, 2 n = 80, 3 n = 120) was found, suggesting meiotic breakdown in their F 1 parent. However, no detectable chromosome rearrangements between parental forms were identified. Genomic instability through aneuploidy thus appears to contribute to reproductive isolation between dwarf and normal lake whitefish, despite their very recent divergence (approx. 15–20 000 generations). Our data suggest that genetic incompatibilities may accumulate early during speciation and limit hybridization between nascent species.

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Cytogenetics of the Simulium arcticum complex (Diptera: Simuliidae)

Zootaxa ◽

10.11646/zootaxa.5039.3.4 ◽

2021 ◽

Vol 5039 (3) ◽

pp. 395-408

Author(s):

GERALD F. SHIELDS

Keyword(s):

Reproductive Isolation ◽

Chromosomal Rearrangements ◽

Geographic Range ◽

Reproductive Status ◽

Data Sets ◽

Black Flies ◽

Data Set ◽

Northern Mexico ◽

Chromosomal Data ◽

The Many

Descriptions of chromosomal rearrangements, geographic distributions and frequencies of nine siblings and 28 cytotypes of the Simulium arcticum Malloch complex are presented. Findings are based on six data sets that include approximately 21,000 chromosomally analyzed larvae from throughout the known geographic range of S. arcticum. This is the largest chromosomal data set for any North American complex of black flies. This summary emphasizes the need to chromosomally analyze taxa of black flies since this type of analysis can result in, not only, a better understanding of the number of taxa in a complex and their relationships but also, it may help to understand the initial stages of reproductive isolation within otherwise morphologically identical groups. Geographically, the streams of eastern Alaska, the entire province of the Yukon and northern Mexico should be sampled. Taxonomically the many cytotypes should be tested for reproductive status when they occur in sympatry with other siblings and cytotypes of the complex. Finally, comparative multi-omic research would be useful.

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The strength and genetic basis of reproductive isolating barriers in flowering plants

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2008.0064 ◽

2008 ◽

Vol 363 (1506) ◽

pp. 3009-3021 ◽

Cited By ~ 320

Author(s):

David B Lowry ◽

Jennifer L Modliszewski ◽

Kevin M Wright ◽

Carrie A Wu ◽

John H Willis

Keyword(s):

Reproductive Isolation ◽

Chromosomal Rearrangements ◽

Variable Number ◽

Future Research ◽

Relative Role ◽

Postzygotic Isolation ◽

Direct Role ◽

Evolutionary Forces ◽

Geographical Scale

Speciation is characterized by the evolution of reproductive isolation between two groups of organisms. Understanding the process of speciation requires the quantification of barriers to reproductive isolation, dissection of the genetic mechanisms that contribute to those barriers and determination of the forces driving the evolution of those barriers. Through a comprehensive analysis involving 19 pairs of plant taxa, we assessed the strength and patterns of asymmetry of multiple prezygotic and postzygotic reproductive isolating barriers. We then reviewed contemporary knowledge of the genetic architecture of reproductive isolation and the relative role of chromosomal and genic factors in intrinsic postzygotic isolation. On average, we found that prezygotic isolation is approximately twice as strong as postzygotic isolation, and that postmating barriers are approximately three times more asymmetrical in their action than premating barriers. Barriers involve a variable number of loci, and chromosomal rearrangements may have a limited direct role in reproductive isolation in plants. Future research should aim to understand the relationship between particular genetic loci and the magnitude of their effect on reproductive isolation in nature, the geographical scale at which plant speciation occurs, and the role of different evolutionary forces in the speciation process.

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Natural selection and intrinsic barriers play important roles in speciation of two closely related Populus (Salicaceae) species

10.22541/au.161251070.07552202/v1 ◽

2021 ◽

Author(s):

Yang Tian ◽

Shuyu Liu ◽

Pär Ingvarsson ◽

Dandan Zhao ◽

Li Wang ◽

...

Keyword(s):

Natural Selection ◽

Reproductive Isolation ◽

Chromosomal Rearrangements ◽

Tibet Plateau ◽

Sequencing Data ◽

Genome Wide ◽

Genomic Divergence ◽

Or Gene ◽

Highly Correlated ◽

Qinghai Tibet Plateau

Despite the growing number of recent studies on genome-wide divergence during speciation, the genetic basis and mechanisms of genomic divergence are still incompletely understood. In most species, natural selection plays a key role in heterogeneous genomic divergence. Additionally, intrinsic barriers, such as chromosomal rearrangements or gene incompatibilities, can also cause genomic heterogeneity. Based on whole genome re-sequencing data from 27 Populus alba and 28 P. adenopoda individuals, we explored the reasons for heterogeneous genomic divergence of these two closely related species. The results showed that the two species diverged ~5-10 million years ago (Mya), when the Qinghai-Tibet Plateau reached a certain height and the inland climate of the Asian continent became arid, which is associated with the fact that the two species begin to diverge and eventually led to speciation. In highly differentiated regions, the absolute divergence (dxy) was significantly higher than genomic background, and relative and absolute divergence were highly correlated, which indicates that intrinsic barriers played an important role in maintaining genomic heterogeneous divergence. Additionally, θπ and shared polymorphisms decreased while fixed differences increased in highly differentiated regions, which are characteristics of natural selection. The above description indicates that the combination of intrinsic barriers and natural selection result in heterogeneous genomic divergence and reproductive isolation. We further found some genes that are related to reproduction may be involved in explaining the reproductive isolation of the two species.

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Genetic analysis of hybrid incompatibility suggests transposable elements increase reproductive isolation in the D. virilis clade

10.1101/753814 ◽

2019 ◽

Author(s):

Dean M. Castillo ◽

Leonie C. Moyle

Keyword(s):

Transposable Elements ◽

Reproductive Isolation ◽

Interspecific Cross ◽

Drosophila Virilis ◽

Interspecific Crosses ◽

Closely Related Species ◽

Hybrid Incompatibility ◽

Alternative Hypotheses ◽

Hybrid Dysfunction

AbstractAlthough observed in many interspecific crosses, the genetic basis of most hybrid incompatibilities is still unknown. Mismatches between parental genomes in selfish elements and the genes that regulate these elements are frequently hypothesized to underlie hybrid dysfunction. We evaluated the potential role of transposable elements (TEs) in hybrid incompatibilities by examining hybrids between Drosophila virilis strains polymorphic for TEs that cause dysgenesis and a closely related species that appears to lack these elements. Using genomic data, we confirmed copy number differences in potentially causal TEs between the dysgenic-causing D. virilis (TE+) strain and a sensitive D. virilis (TE-) strain and D. lummei genotype. We then contrasted isolation phenotypes in a cross where dysgenic TEs are absent from both D. virilis (TE-) and D. lummei parental genotypes, to a cross where dysgenic TEs are present in the D. virilis (TE+) parent and absent in the D. lummei parent, predicting increased reproductive isolation in the latter cross. Using F1 and backcross experiments that account for alternative hypotheses, we demonstrated amplified reproductive isolation specifically in the interspecific cross involving TE+ D. virilis, consistent with the action of dysgenesis-inducing TEs. These experiments demonstrate that TEs can contribute to hybrid incompatibilities via presence/absence polymorphisms.

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