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The mitonuclear compatibility species concept (1 Viewer)

this seems to just be a derivation of the phylogenetic species concept, only relying upon only mitochondrial DNA. This strikes me as a concept that isn't going to get a lot of support in the bird world.
 
Conceptually, I would rather see it as a highly reductory and specialized derivation of the BSC, actually.
MCSC: "A species is a population that is genetically isolated from other populations by incompatibilities in uniquely coadapted mt and NO-mt genes."
...While a gene-based variant of the BSC might be: "A species is a population that is genetically isolated from other populations by incompatibilities", period.
 
This is an interesting concept. I skimmed the paper quick just now, and to address Morgan's thought about this being similar to PSC (which was also my initial thought), I have attached here a screenshot of Table 2 where the author lists the BSC, PSC, and this new concept and how they differ.

As to how much it would make life easier, I don't think it would really make things easier. The author goes through a couple examples where this concept justifies treating things as species that are messy under other concepts (like Blue-winged and Golden-winged Warblers), but he also discusses cases where this concept doesn't seem to fit well (like the problem with Common Raven in western North America).

It is an interesting concept, and I enjoyed skimming through the paper, though, like Morgan, I don't see it as really catching on very much in the bird world, or at least in the more conservative taxonomic bodies like NACC/SACC.
 

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Conceptually, I would rather see it as a highly reductory and specialized derivation of the BSC, actually.
MCSC: "A species is a population that is genetically isolated from other populations by incompatibilities in uniquely coadapted mt and NO-mt genes."
...While a gene-based variant of the BSC might be: "A species is a population that is genetically isolated from other populations by incompatibilities", period.

I agree that MCSC seems to be nearly a subset of BSC in term of its theoretical layout, as does the author - "The central idea of the biological species concept—that species represent discrete gene pools—is also the central tenet of the mitonuclear compatibility species concept (MCSC)". - this despite the author's statement: "In practice, in the great majority of cases, the criteria of the phylogenetic species concept identify the same species boundaries as do the criteria of the MCSC."

The paper seems to rely on some unaddressed assumptions, but most especially that mitonuclear compatibility is THE driver of evolution, and other divergent traits are simply reactions to it. (see the sections on Ornamental Traits and Species Boundaries, Linkages, and interspersed in other sections). I feel that much more evidence would be needed to support that case. Certainly it could be a driver, and very likely is in some cases - but that is not the only reason taxa can be different. Notably missing from the article were much mention of classic speciation drivers like isolation or environmental/niche differences. Polyploid species of plants, mammal, and amphibians would likely be unrecognized under the MSCS concept, as would young species with profound mating strategy differences - I'm thinking insects especially would be ill-suited to this species concept.

In contrast, if there happened to be very successful and retained biochemical solutions to mitonuclear compatibility, those genes my persist "living fossil style" in several taxa that are species under any other concept. The author seems to support the idea that high-metabolism animals such as birds and mammals have such high mitochondrial mutation rates that this is not an issue- but that begs the counterpoint that it would then be an issue for plants, invertebrates, etc.

Also I'm uncomfortable with the presentation in the Mitonuclear Speciation vs. Contemporary Models of Speciation section. The following passage strikes me as having a "chicken-or-the-egg" problem with species definition: "...studies with nematodes, copepods, fruit flies, parasitic wasps, rodents, and primates all show that each species of animal has a unique set of coadapted mt and NO-mt genes. The very important consequence of the rapid divergence of mt and NO-mt genes is that “hybrid” offspring, which result from mating between populations with diverged coadapted gene sets, have reduced fitness due to reduced OXPHOS function resulting from mitonuclear incompatibilities" So we know that mt and NO-mt genes define species because different species have different mt and NO-mt genes?!?!

All that said, this paper is a good contribution and I think the author rightly identifies this concept as one practically ignored in ornithology, yet potentially very important. The Blue-winged/Golden-winged Warbler example seems like an excellent illustration of the utility of this concept, and the Yellow-rumped Warbler analysis struck me as a great application as well. I think the MCSC is useful in species discussion, perhaps as a component to other species concepts, but not as elementary to speciation as the paper seems to imply.
 
Isn't it at the core of it a false assumption that barriers between any species must involve some of a small number of genes?
 
Isn't it at the core of it a false assumption that barriers between any species must involve some of a small number of genes?
You may look at it this way but, strictly speaking, it's not 'an assumption' any more as soon as it's become part of his definition of the word 'species'...
(Any two 'things' separated by barriers others than those involving this small number of genes are not 'species'.)
 
I have not found the time to read the paper - does the author discuss the claims of "mitochondrial sweep" that has been reported?

Niels
 
Sloan, Havird, Sharbrough. 2017. Invited reviews and synthese. The on-again, off-again relationship between mitochondrial genomes and species boundaries. Mol. Ecol. 26(8):2212–2236.
[abstract] [pdf (preprint) here]

Abstract -
The study of reproductive isolation and species barriers frequently focuses on mitochondrial genomes and has produced two alternative and almost diametrically opposed narratives. On one hand, mtDNA may be at the forefront of speciation events, with co-evolved mitonuclear interactions responsible for some of the earliest genetic incompatibilities arising among isolated populations. On the other hand, there are numerous cases of introgression of mtDNA across species boundaries even when nuclear gene flow is restricted. We argue that these seemingly contradictory patterns can result from a single underlying cause. Specifically, the accumulation of deleterious mutations in mtDNA creates a problem with two alternative evolutionary solutions. In some cases, compensatory or epistatic changes in the nuclear genome may ameliorate the effects of mitochondrial mutations, thereby establishing coadapted mitonuclear genotypes within populations and forming the basis of reproductive incompatibilities between populations. Alternatively, populations with high mitochondrial mutation loads may be rescued by replacement with a more fit, foreign mitochondrial haplotype. Coupled with many nonadaptive mechanisms of introgression that can preferentially affect cytoplasmic genomes, this form of adaptive introgression may contribute to the widespread discordance between mitochondrial and nuclear genealogies. Here, we review recent advances related to mitochondrial introgression and mitonuclear incompatibilities, including the potential for cointrogression of mtDNA and interacting nuclear genes. We also address an emerging controversy over the classic assumption that selection on mitochondrial genomes is inefficient and discuss the mechanisms that lead lineages down alternative evolutionary paths in response to mitochondrial mutation accumulation.
 
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McDiarmid, C. S., Hooper, D. M., Stier, A., & Griffith, S. C. (2024). Mitonuclear interactions impact aerobic metabolism in hybrids and may explain mitonuclear discordance in young, naturally hybridizing bird lineages. Molecular Ecology, 00, e17374. https://doi.org/10.1111/mec.17374

Understanding genetic incompatibilities and genetic introgression between incipient species are major goals in evolutionary biology. Mitochondrial genes evolve rapidly and exist in dense gene networks with coevolved nuclear genes, suggesting that mitochondrial respiration may be particularly susceptible to disruption in hybrid organisms. Mitonuclear interactions have been demonstrated to contribute to hybrid dysfunction between deeply divergent taxa crossed in the laboratory, but there are few empirical examples of mitonuclear interactions between younger lineages that naturally hybridize. Here, we use controlled hybrid crosses and high-resolution respirometry to provide the first experimental evidence in a bird that inter-lineage mitonuclear interactions impact mitochondrial aerobic metabolism. Specifically, respiration capacity of the two mitodiscordant backcrosses (with mismatched mitonuclear combinations) differs from one another, although they do not differ significantly from the parental groups or mitoconcordant backcrosses as we would expect of mitonuclear disruptions. In the wild hybrid zone between these subspecies, the mitochondrial cline centre is shifted west of the nuclear cline centre, which is consistent with the direction of our experimental results. Our results therefore demonstrate asymmetric mitonuclear interactions that impact the capacity of cellular mitochondrial respiration and may help to explain the geographic discordance between mitochondrial and nuclear genomes observed in the wild.
 
McDiarmid, C. S., Hooper, D. M., Stier, A., & Griffith, S. C. (2024). Mitonuclear interactions impact aerobic metabolism in hybrids and may explain mitonuclear discordance in young, naturally hybridizing bird lineages. Molecular Ecology, 00, e17374. https://doi.org/10.1111/mec.17374

Understanding genetic incompatibilities and genetic introgression between incipient species are major goals in evolutionary biology. Mitochondrial genes evolve rapidly and exist in dense gene networks with coevolved nuclear genes, suggesting that mitochondrial respiration may be particularly susceptible to disruption in hybrid organisms. Mitonuclear interactions have been demonstrated to contribute to hybrid dysfunction between deeply divergent taxa crossed in the laboratory, but there are few empirical examples of mitonuclear interactions between younger lineages that naturally hybridize. Here, we use controlled hybrid crosses and high-resolution respirometry to provide the first experimental evidence in a bird that inter-lineage mitonuclear interactions impact mitochondrial aerobic metabolism. Specifically, respiration capacity of the two mitodiscordant backcrosses (with mismatched mitonuclear combinations) differs from one another, although they do not differ significantly from the parental groups or mitoconcordant backcrosses as we would expect of mitonuclear disruptions. In the wild hybrid zone between these subspecies, the mitochondrial cline centre is shifted west of the nuclear cline centre, which is consistent with the direction of our experimental results. Our results therefore demonstrate asymmetric mitonuclear interactions that impact the capacity of cellular mitochondrial respiration and may help to explain the geographic discordance between mitochondrial and nuclear genomes observed in the wild.
I'm probably being a bit thick here (or to put it another way molecular biology has advanced considerably since I studied it in the early 70s) but if mitochondria are only inherited through the maternal line, then how can mitochondrial genes be anything other than maternal genes and so why would they be less functional in hybrids?
 
I'm probably being a bit thick here (or to put it another way molecular biology has advanced considerably since I studied it in the early 70s) but if mitochondria are only inherited through the maternal line, then how can mitochondrial genes be anything other than maternal genes and so why would they be less functional in hybrids?
The idea behind this paper and in the broader mitonuclear compatibility concept is that hybrids are theoretically disadvantaged as the mitochondrial and nuclear genes don't work together as well as they would in in the parental species. I'm no mechanic, but I liken it to putting a Ferrari engine in a Ford Focus. It'll probably work for a while, but eventually it'll blow a gasket.
 
I'm probably being a bit thick here (or to put it another way molecular biology has advanced considerably since I studied it in the early 70s) but if mitochondria are only inherited through the maternal line, then how can mitochondrial genes be anything other than maternal genes and so why would they be less functional in hybrids?

Genes do migrate between mitochondrial and nuclear genomes over evolutionary time. Mitochondria are no longer capable of free living because some vital genes are now in the nucleus (e.g. some involved in oxidative phosphorylation).

This means for proper functioning of mitochondria, notably respiration, they require some nuclear genes. Nuclear genes encoding mitochondrial proteins from the maternal line will match the mitochondrial genes because they have co-evolved, while those from the paternal line may not be as well matched, meaning their will be selection pressures in favour of the maternal nuclear genes.
 

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