“Ghost Introgression” As a Cause of Deep Mitochondrial Divergence in a Bird Species Complex

Zhang, Dezhi; Tang, Linfang; Cheng, Yanhao; Hao, Yan; Xiong, Ying; Song, Gang; Qu, Yanhua; Rheindt, Frank E.; Alström, Per; Jia, Chenxi; Lei, Fumin

doi:10.1093/molbev/msz170

Cited by 83 publications

(73 citation statements)

References 62 publications

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“…This would happen through the dynamics of drift that western populations experience at their invasion front. A result is an mtDNA disjunction or mtDNA‐defined zone of contact extending deeper and deeper into the western population's current geographical range (see examples in Seixas, Boursot, & Melo‐Ferreira, 2018; Zhang et al., 2019). Here, this mtDNA disjunction is therefore expected to be west of the current zones of admixture as measured primarily in nuclear DNA characters (Figure 2) but also in phenotypic characters (Black et al., 2019; Figure 1).…”

Section: Discussionmentioning

confidence: 99%

Robbery in progress: Historical museum collections bring to light a mitochondrial capture within a bird species widespread across southern Australia, the Copperback Quail‐thrush Cinclosoma clarum

McElroy

Black

Dolman

et al. 2020

Ecology and Evolution

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We surveyed mitochondrial, autosomal, and Z chromosome diversity within and between the Copperback Quail‐thrush Cinclosoma clarum and Chestnut Quail‐thrush C. castanotum, which together span the arid and semi‐arid zones of southern Australia, and primarily from specimens held in museum collections. We affirm the recent taxonomic separation of the two species and then focus on diversity within the more widespread of the two species, C. clarum. To guide further study of the system and what it offers to understanding the genomics of the differentiation and speciation processes, we develop and present a hypothesis to explain mitonuclear discordance that emerged in ourdata. Following a period of historical allopatry, secondary contact has resulted in an eastern mitochondrial genome replacing the western mitochondrial genome in western populations. This is predicted under a population‐level invasion in the opposite direction, that of the western population invading the range of the eastern one. Mitochondrial captures can be driven by neutral, demographic processes, or adaptive mechanisms, and we favor the hypothesized capture being driven by neutral means. We cannot fully reject the adaptive process but suggest how these alternatives may be further tested. We acknowledge an alternative hypothesis, which finds some support in phenotypic data published elsewhere, namely that outcomes of secondary contact have been more complex than our current genomic data suggest. Discriminating and reconciling these two alternative hypotheses, which may not be mutually exclusive, could be tested with closer sampling at levels of population, individual, and nucleotide than has so far been possible. This would be further aided by knowledge of the genetic basis to phenotypic variation described elsewhere.

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Section: Discussionmentioning

confidence: 99%

Robbery in progress: Historical museum collections bring to light a mitochondrial capture within a bird species widespread across southern Australia, the Copperback Quail‐thrush Cinclosoma clarum

McElroy

Black

Dolman

et al. 2020

Ecology and Evolution

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“…Patterns of deep divergence in organellar DNA in combination with shallow nuclear divergence might be due to mitochondrial or plastid capture from an extinct species. [ 8–10 ] However, other demographic and evolutionary processes—including sex‐biased gene flow, [ 11 ] androgenesis, [ 12 ] genetic drift [ 13 ] or independent sorting of haplotypes in a large population [ 14 ] —can culminate in similar patterns. Therefore, it is advisable to rule out these alternative explanations and provide additional evidence for introgression from an extinct lineage, such as signatures of ghost introgression in the nuclear genome.…”

Section: Ghostbusters: Detecting Ghost Introgressionmentioning

confidence: 99%

“…Subsequent analyses of the nuclear genome uncovered several highly diverged regions that were considered remnants of the ancient hybridization events that also resulted in the mtDNA transfer. [ 8 ]…”

Section: Ghostbusters: Detecting Ghost Introgressionmentioning

confidence: 99%

“…In summary, deeply divergent haplotypes often provide the first clue for the presence of introgression from an extinct lineage. [ 8,15 ] The hypothesis of ghost introgression can be further explored with more sophisticated methods (e.g., S* statistic and hidden Markov models) that pinpoint putatively introgressed regions. [ 17,19 ] Finally, different demographic models can be compared in a statistical framework to confirm or reject the existence of ghost introgression.…”

Section: Ghostbusters: Detecting Ghost Introgressionmentioning

confidence: 99%

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Ghost Introgression: Spooky Gene Flow in the Distant Past

Ottenburghs

2020

BioEssays

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Evolution is a continuous trial and error process in which most lineages go extinct without leaving fossil remains. Many of these lineages would be closely related and occasionally hybridized with lineages that gave rise to extant species. Hence, it is likely that one can find genetic signatures of these ancient introgression events in present-day genomes, so-called ghost introgression. The increasing availability of high-quality genome assemblies for non-model organisms and the development of more sophisticated methods for detecting introgression will undoubtedly reveal more cases of ghost introgression, indicating that the Tree of Life is even more reticulated than assumed. The presence of ghost introgression has important consequences for the study of numerous evolutionary processes, including adaptation, speciation, and macroevolutionary patterns. In addition, detailed studies of introgressed regions could provide insights into the morphology of the extinct lineage, providing an unexpected link between genomics and the fossil record. Hence, new methods that take into account ghost introgression will need to be developed.

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“…Using phylogenetic reconstruction, we observed a complex evolutionary history of mitochondria in D. paulistorum, with both ancient and recent introgressions. We suggest that an a-like mitochondrion was the ancestral mitotype of the species and that heteroplasmy might have originated through introgression of the b mitotype from an unsampled or extinct donor, a concept known as 'ghost' introgression [55][56][57]. We speculate that the unusual biparental transmission mode of a2 might have developed through competition with the b mitochondria for maternal transmission.…”

Section: Introductionmentioning

confidence: 89%

Multiple introgressions shape mitochondrial evolutionary history inDrosophila paulistorumand theDrosophila willistonigroup

Baião

Strunov

Heyworth

et al. 2020

Preprint

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Heteroplasmy is the coexistence of more than one type of mitochondria in an organism. Although widespread sequencing has identified several cases of transient or low-level heteroplasmy that primarily occur through mutation or paternal leakage, stable, high-titer heteroplasmy remains rare in animals. In this study we present a unique, stable and high-level heteroplasmy in male and female flies belonging to the neotropical Drosophila paulistorum species complex. We show that mitochondria of D. paulistorum are polyphyletic and form two clades, α and β, with two subclades each. Mitochondria of the α2 subclade appear functional based on their genomic integrity but are exclusively found in heteroplasmic flies and never in homoplasmy, suggesting that they are a secondary mitotype with distinct functionality from the primary mitochondria. Using qPCR, we show that α2 titer do not respond to energetic demands of the cell and are generally higher in males than females. By crossing hetero- and homoplasmic flies, we find that α2 can be transmitted to their offspring via both parents and that levels are dependent on nuclear background. Following α2 mitotype levels during embryogenesis, we demonstrate that this secondary mitotype replicates rapidly just after fertilization of the egg in a period when primary mitochondria are dormant. This so-called “Replication precox” mitochondrial phenotype likely prevents the α2 mitotype from being outcompeted by the primary mitotype – and thereby secures its persistence and further spread as a selfish mitochondrion, we hereby designate “Spartacus”. Finally, we reconstruct the evolutionary history of mitochondria in the willistoni subgroup uncovering signs of multiple mitochondrial losses and introgressions. Our data indicate an α-like mitochondrial ancestor in the willistoni subgroup, with the β mitotype likely acquired via introgression from an unidentified donor. We hypothesize that the selfish characteristics of α2 might have emerged as a response to competition for inheritance with the introgressed β mitotype.

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“Ghost Introgression” As a Cause of Deep Mitochondrial Divergence in a Bird Species Complex

Cited by 83 publications

References 62 publications

Robbery in progress: Historical museum collections bring to light a mitochondrial capture within a bird species widespread across southern Australia, the Copperback Quail‐thrush Cinclosoma clarum

Robbery in progress: Historical museum collections bring to light a mitochondrial capture within a bird species widespread across southern Australia, the Copperback Quail‐thrush Cinclosoma clarum

Ghost Introgression: Spooky Gene Flow in the Distant Past

Multiple introgressions shape mitochondrial evolutionary history inDrosophila paulistorumand theDrosophila willistonigroup

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