A test for meiotic drive in hybrids between Australian and Timor zebra finches

Knief, Ulrich; Forstmeier, Wolfgang; Pei, Yifan; Wolf, Jochen B. W.; Kempenaers, Bart

doi:10.1002/ece3.6951

Cited by 3 publications

(3 citation statements)

References 87 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…It has been demonstrated that divergence of centromeric sequences between species may lead to female meiotic drive in interspecific hybrids ( Chmátal et al, 2014 ; Akera et al, 2019 ; Knief et al, 2020 ). Theoretically, the divergence of centromeres could, in an extreme case, also cause the sterility of female hybrids and thus contribute to reproductive isolation between species ( Hurst and Pomiankowski, 1991 ; Phadnis and Orr, 2009 ; Zhang et al, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

Comparison of Karyotypes in Two Hybridizing Passerine Species: Conserved Chromosomal Structure but Divergence in Centromeric Repeats

et al. 2021

View full text Add to dashboard Cite

Changes in chromosomal structure involving chromosomal rearrangements or copy number variation of specific sequences can play an important role in speciation. Here, we explored the chromosomal structure of two hybridizing passerine species; the common nightingale (Luscinia megarhynchos) and the thrush nightingale (Luscinia luscinia), using conventional cytogenetic approaches, immunostaining of meiotic chromosomes, fluorescence in situ hybridization as well as comparative genomic hybridization (CGH). We found that the two nightingale species show conserved karyotypes with the same diploid chromosome number of 2n = 84. In addition to standard chromosomes, both species possessed a small germline restricted chromosome of similar size as a microchromosome. Just a few subtle changes in chromosome morphology were observed between the species, suggesting that only a limited number of chromosomal rearrangements occurred after the species divergence. The interspecific CGH experiment suggested that the two nightingale species might have diverged in centromeric repetitive sequences in most macro- and microchromosomes. In addition, some chromosomes showed changes in copy number of centromeric repeats between the species. The observation of very similar karyotypes in the two nightingale species is consistent with a generally slow rate of karyotype evolution in birds. The divergence of centromeric sequences between the two species could theoretically cause meiotic drive or reduced fertility in interspecific hybrids. Nevertheless, further studies are needed to evaluate the potential role of chromosomal structural variations in nightingale speciation.

show abstract

Section: Discussionmentioning

confidence: 99%

Comparison of Karyotypes in Two Hybridizing Passerine Species: Conserved Chromosomal Structure but Divergence in Centromeric Repeats

et al. 2021

View full text Add to dashboard Cite

show abstract

“…Presumably because females of wild-derived guttata birds do not easily reproduce in captivity, we hypothesized that guttata males were crossed with an already domesticated castanotis female (from Europe), and the resulting female hybrids were back crossed with pure guttata males for about five generations (P-BC5) until the population was phenotypically guttata -like. This reconstruction is based on the genotyping of one male ( 49 ) of the resulting hybrid population (yellow background, Bottom ), which is characterized by a castanotis mother contributing the mtDNA (dark blue circle), the female-specific W chromosome (dark blue short rectangle; for details, see SI Appendix , Results ), and 5% of the A-chromosomal DNA (blue fragments in the long rectangles) and guttata males contributing 95% of the A-chromosomal DNA (orange-brown long rectangles) and the GRC (orange-brown sigmoid symbol). Note that the paternal inheritance of the GRC must have happened sometime between generations P and BC5 (solid arrow with asterisk).…”

Section: Resultsmentioning

confidence: 99%

Occasional paternal inheritance of the germline-restricted chromosome in songbirds

Pei

Forstmeier

Ruiz‐Ruano

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

View full text Add to dashboard Cite

Songbirds have one special accessory chromosome, the so-called germline-restricted chromosome (GRC), which is only present in germline cells and absent from all somatic tissues. Earlier work on the zebra finch (Taeniopygia guttata castanotis) showed that the GRC is inherited only through the female line—like the mitochondria—and is eliminated from the sperm during spermatogenesis. Here, we show that the GRC has the potential to be paternally inherited. Confocal microscopy using GRC-specific fluorescent in situ hybridization probes indicated that a considerable fraction of sperm heads (1 to 19%) in zebra finch ejaculates still contained the GRC. In line with these cytogenetic data, sequencing of ejaculates revealed that individual males from two families differed strongly and consistently in the number of GRCs in their ejaculates. Examining a captive-bred male hybrid of the two zebra finch subspecies (T. g. guttata and T. g. castanotis) revealed that the mitochondria originated from a castanotis mother, whereas the GRC came from a guttata father. Moreover, analyzing GRC haplotypes across nine castanotis matrilines, estimated to have diverged for up to 250,000 y, showed surprisingly little variability among GRCs. This suggests that a single GRC haplotype has spread relatively recently across all examined matrilines. A few diagnostic GRC mutations that arose since this inferred spreading suggest that the GRC has continued to jump across matriline boundaries. Our findings raise the possibility that certain GRC haplotypes could selfishly spread through the population via occasional paternal transmission, thereby outcompeting other GRC haplotypes that were limited to strict maternal inheritance, even if this was partly detrimental to organismal fitness.

show abstract

“…Presumably because females of wild-derived guttata birds do not easily reproduce in captivity, we hypothesize that guttata males were crossed with an already domesticated castanotis female (from Europe), and the resulting female hybrids were back-crossed with pure guttata males for about five generations (P-BC5) until the population was phenotypically guttata -like. This reconstruction is based on the genotyping of one male 52 of the resulting hybrid population (yellow background, bottom), which is characterized by a castanotis mother contributing the mtDNA (dark blue circle), the female-specific W-chromosome (dark blue short rectangle; see Supplementary Results ) and 5% of the A-chromosomal DNA (blue fragments in the long rectangles), and guttata males contributing 95% of the A-chromosomal DNA (orange-brown long rectangles) and the GRC (orange-brown sigmoid symbol). Note that the paternal spillover of the GRC must have happened sometime between generations P and BC5 (solid arrow with asterisk).…”

Section: Paternal Inheritance Of the Grc In A Hybrid Populationmentioning

confidence: 99%

Occasional paternal inheritance of the germline-restricted chromosome in songbirds

Pei

Forstmeier

Ruiz‐Ruano

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

All songbirds have one special accessory chromosome1–4, the so-called germline-restricted chromosome (GRC)4–7, which is only present in germline cells and absent from all somatic tissues. Earlier work on the zebra finch (Taeniopygia guttata castanotis) showed that the GRC is inherited only through the female line4,6,8,9 – like mitochondrial DNA7,9–12 – and is eliminated from the sperm during spermatogenesis5,7,9–11. Here we show that the GRC can also be paternally inherited. Confocal microscopy using GRC-specific FISH probes indicated that a considerable fraction of sperm heads (1-19%) in zebra finch ejaculates still contained the GRC. In line with these cytogenetic data, sequencing of ejaculates revealed that individual males from two families differed strongly and consistently in the number of GRCs in their ejaculates. Examining a captive-bred population of hybrids of the two zebra finch subspecies (T. g. guttata and T. g. castanotis) revealed that the descendants inherited their mitochondria from a castanotis mother but their GRC from a guttata father. Moreover, GRC haplotypes across nine different castanotis matrilines showed at best a weak tendency to be co-inherited with mtDNA haplotypes. Within castanotis, the GRC showed little variability, while the mtDNA of matrilines was highly divergent. This suggests that a single GRC haplotype has recently spread across the entire castanotis population, crossing the matriline boundaries via paternal spillover. Our findings raise the possibility that certain GRC haplotypes could selfishly spread through the population, via additional paternal transmission, thereby outcompeting other GRC haplotypes that were limited to strict maternal inheritance, even if this was partly detrimental to organismal fitness.

show abstract

A test for meiotic drive in hybrids between Australian and Timor zebra finches

Cited by 3 publications

References 87 publications

Comparison of Karyotypes in Two Hybridizing Passerine Species: Conserved Chromosomal Structure but Divergence in Centromeric Repeats

Comparison of Karyotypes in Two Hybridizing Passerine Species: Conserved Chromosomal Structure but Divergence in Centromeric Repeats

Occasional paternal inheritance of the germline-restricted chromosome in songbirds

Occasional paternal inheritance of the germline-restricted chromosome in songbirds

Contact Info

Product

Resources

About