Mitochondrial male sterility

Most plants are hermaphrodites, producing both pollen and seeds, but there are many species in which some individuals are morphodites and others are purely female.  Often this femaleness (male sterility) is caused by a mitochondrial mutation.

I once heard Bob Trivers explain this: it’s simple and interesting.  Hermaphroditic individuals often self-fertilize, which is a gift and a curse. It’s a gift because seeds from self-fertilization have two copies of the plant’s genome, rather than one: fitness is increased, all else equal.  It’s a curse because of inbreeding depression: lots of homozygosity makes one weak.  From the plant’s point of view, having two sexes and selfing is a good thing as long as the extent of inbreeding depression is less than one-half.  But mitochondria are only transmitted maternally, and  so have nothing to gain from inbreeding- no extra copies get transmitted. While they suffer from being inside inbred, gap-toothed seeds.  So,  any mitochondrial mutation that prevents selfing (by eliminating pollen production) increases mitochondrial fitness, while generally reducing nuclear gene fitness.

Also, energy spent on pollen production is now available for making more seeds, but that’s a secondary effect, usually.

 

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24 Responses to Mitochondrial male sterility

  1. melendwyr says:

    What’s truly interesting is that sometimes if the mitochrondrial strain is transplanted into another strain of the host plant, the result is pollen-fertile. It seems the problem isn’t always with the genes themselves, but compatibilities between the genomes of the host and the symbiote.

    I’ve also heard that the issues can arise from chloroplasts as well as mitochrondria, since both have their own genomes, although that’s not an issue with pollen fertility as such.

    And then there are the plants where the infertility sometimes stems from complex developmental problems which weren’t selected out due to vegetative cloning being used to propagate the species… like with garlic. Infertile plants produce bigger cloves, so we selected for problems. Happily the effect can be partially reversed with intervention, and several generations of seed production seem to select for fertile combinations again.

  2. reiner Tor says:

    But why do mitochondria allow for males to be formed? They could increase their fitness in the short run by only producing females. Is it possible that women whose mothers and maternal grandmothers etc. only produced daughters for several generations couldn’t find husbands, or only less worthy husbands? I guess it must be so. But how is it prevented at present? If there was a mutation in mitochondria which only allowed for the production of female zygotes, such mutation would spread in our present society where people care for neither the sex of the child nor the family history of the prospective spouse.

    • melendwyr says:

      It’s usually cheaper to be a male than a female. All else being equal, males can spread their genes more widely than females with the same resources. So strains that happen to develop a resistance to pollen fertility end up dominating the genome. Perhaps there’s a Red Queen’s Race going on, with subtle competition between host and symbiote.

      Consider also that if a female-only line dominated a locale enough, there wouldn’t be any males to fertilize and that strain would likely fail to reproduce. If populations aren’t so evenly distributed as to form one large breeding pool, such traits might constantly arise and then die out. (If the strain happened to be parthogenic, like triploid dandelions are, they might establish an entire new subspecies.)

      It’s also worth noting that the incompatibilities that lead to pollen sterility are thought to also induce subtle inefficiencies in metabolism generally.

    • RCB says:

      The spread of mitochondrial male sterility alters the sex ratio. This imposes a strong selective pressure on nuclear genes to produce more males, as males will then produce a larger mean number of nuclear genetic descendants. Classic Fisherian theory. So for every mitoch. sterile gene that arises, we should see a nuclear gene arise that suppresses it…. Eventually.

      I recall seeing a paper suggesting that a disproportionate number of sperm defects come from mitochondrial mutations. This makes a lot of sense.

      • reiner Tor says:

        Thanks, sounds like a good explanation.

        • RCB says:

          At a more proximate level, I suspect it’s pretty hard to shut off male production in humans without producing some pretty bad pleiotropic effects. Dinging sperm is one thing, but I find it hard to imagine that a mitochondrial mutation could arise that selectively aborts male fetuses but do nothing else bad. Maybe I’m just not very imaginative.

          • melendwyr says:

            Since fetuses are female by default, and IIRC there’s a gene on the Y-chromosome that triggers the transformation into maleness, it seems like a mutation there could easily shut down the entire process.

            Eliminating males would be simple. Keeping the species going without them, though… not so much.

          • RCB says:

            Melendwyr –
            A mutation on the Y chromosome that suppressed maleness would have no selective advantage.

            Is there a simple mutation in the mitochondrial DNA that could do it?

  3. RCB says:

    Burt and Trivers’s book Genes in Conflict is the place to go for this stuff. The charlesworth’s new-ish evolutionary genetics text book also models it. The models I’ve seen always supposed that the added seed production was the primary benefit. Is there evidence that the inbreeding avoidance mechanism is more important?

    • gcochran9 says:

      Inbreeding depression is a big effect, not hard for it to dominate. Perhaps more likely with some plant that has its pollen spread by bees and thus doesn’t have to make that much pollen in the first place.

      • RCB says:

        I suppose one prediction would be that mitochondrial male sterility alleles would be more common in taxa that do lots of selfing. E.g. grasses, annuals. If inbreeding avoidance is the main explanation, then an MMS mutation wouldn’t provide any benefit to the mitochondria in plants that already are well guarded against selfing. It’s tricky though, because selfing evolves adaptively too, e.g. as pollen assurance. So maybe it’s more complicated than that.

        • Thank you RCB for the book recommendation. I just ordered it along with seven books Cochran just recently recommended back around Christmas. Amazon charges me $4 per delivery to my doorstep and a pittance per book. Nobody has any excuse anymore why they can’t build up a collection of good books, it is too easy and too cheap. Unless of course they keep giving them away to friends like I do. Maybe I’m just an old fart but I don’t like kindle versions. Now all I need is lots of free time.

          • Patrick Boyle says:

            I agree. I read Kindle for a while but now I tend to only read used books. For example I’m reading a book on mitochondria right now called ‘Power, Sex. Suicide – Mitochondria and the Meaning of Life.’. The books are almost always nearly perfect and they are very cheap. The only drawback is that they come through the mail randomly rather than promptly.

            At four dollars a book I buy on impulse and throw away the losers.

  4. The fourth doorman of the apocalypse says:

    Sperm, of course, contain mitochondria, just many fewer than normal somatic cells and ova. It seems that in most cases, the father’s mitochondria in his sperm never make it into the zygote and some claim it is rejected, although I saw a reference somewhere of a man who carried his father’s mitochondria (possibly along with his mother’s.)

    • The fourth doorman of the apocalypse says:

      I also read a report somewhere of a man in China who was alleged to have a karyotype of 42XY, It seems that he had Robertsonian translocations on both chromosomes of one pair. If he could somehow find a person whose karyotype is 42XX he could start a new species.

    • The fourth doorman of the apocalypse says:

      Interesting paper here:

      Sperm Mitochondria in Reproduction: Good or Bad and Where Do They Go?

      Abstract excerpt:

      … The viewpoints that sperm bearing more mtDNA will have a better fertilizing capability and that sperm mtDNA is actively eliminated during early embryogenesis are widely accepted. However, this may be not true for several mammalian species, including mice and humans. Here, we review the sperm mitochondria and their mtDNA in sperm functions, and the mechanisms of maternal mitochondrial inheritance in mammals.

  5. ziel says:

    It’s a Gift, The Bank Dick, and My Little Chickadee are all top-notch Fields efforts. They all show up on Turner Classic Movies from time-to-time. I haven’t seen the other two in ages so can’t comment on them. I love when I ask a Millennial “Do you like W.C. Fields- do you think he’s funny?” and invariably get the response “Who’s W.C. Fields?”

  6. carol2000 says:

    Maybe my last remaining Texas sage plant has this problem – lots of flowers but no pollen, thus no seeds. They normally self-pollinate very well.

  7. melendwyr says:

    The idea that self-fertilization necessarily leads to inbreeding depression simply doesn’t hold, at least when it comes to plants. Many of our crop plants show little-to-no inbreeding depression and can pollinate themselves indefinitely.

    The probable reason most wild species of plants work to avoid self-fertilization – whether through self-infertility, dual sexes, staggered bloom periods, or so on – is that outbreeding preserves a genetic library of variation while inbreeding leads to uniformity that severely limits future adaptation.

    • gcochran9 says:

      “Inbreeding Depression

              With some exceptions, inbreeding reduces offspring fitness in essentially all naturally outcrossing plants and to a lesser extent in selfing species. The negative effects of mating between relatives have been noticed for many centuries. The careful breeding studies of Darwin (1876) first empirically demonstrated inbreeding depression in a wide variety of taxa. The negative effects of inbreeding have since been observed in both outcrossing and selfing species for a variety of traits with consequences for offspring fitness (Charlesworth and Charlesworth 1987, Keller and Waller 2002). Examples of traits shown to be subjects to inbreeding depression include pollen quantity, number of ovules, amount of seed, germination rate, growth rate and competitive ability (Keller and Waller 2002, Frankham et al. 2003). Genetic models have been developed to functionally explain reduction in fitness-related traits caused by inbreeding."
      
      • melendwyr says:

        Peas. Beans. Squash. Wheat. Virtually all ‘modern’ varieties of tomatoes. They can be perpetuated indefinitely without outcrossing.

        Many vegetables show little to no inbreeding depression, and hybrids between different genetic lines of those species aren’t strongly superior. Gardeners trying to maintain a ‘heirloom’ strain often have to plant up to twenty specimens to hedge against the possibility of a cross.

    • RCB says:

      The reason many selfing plants (and domesticates) show little inbreeding depression is precisely because they do a lot of selfing. Selfing exposes rare deleterious recessives, which normally are nearly invisible to selection. This means that high inbreeding eventually selects out (or “purges”) the rare deleterious recessives that make inbreeding a bad idea in the first place.

      The problem here is that it’s hard to get inbreeding started: sure, it might be okay many generations from now, but in the mean time it will usually be disfavored (this is also why your “maintaining genetic variation” argument probably isn’t the main explanation – it relies on potential future payoffs to the lineage). The main explanation I’ve heard for selfing (apart from the 2x allele advantage) is that it allows reproductive insurance. If you’re a widely dispersing plant on the edge of your species range, you might not be able to find a mate (you can’t get up a look for it – have to rely on pollinators / wind). Producing inbred offspring is better than producing none at all, so some selfing can be adaptive. I believe this is why short-lived, colonizing, annual grasses tend to have higher selfing rates – a well documented phenomenon, I think.

      • melendwyr says:

        Your objection to future benefits is invalid. Life has had a long, long time to work within – the short-term strategies died out long ago.

        It’s relatively easy to eliminate both deleterious recessives and restraints against selfing. If it were advantageous, more organisms would use the strategy. The reality that selfing is only sometimes resorted to, and that most species are designed to make it as unlikely as possible, strongly suggests that the purported benefits don’t exist.

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