Tuesday, May 19, 2009

Sciara and the problems of sex

At the risk of getting too far afield, I want to talk about one of the craziest animals around with respect to transmission genetics. I promise to bring this post back around to bacteria in the future.

The sciarid flies (fungus gnats) illustrate some of the most tantilizing mysteries of genetics in one compact package. When I first learned about the fungus gnats, I found them interesting from the perspective of chromosome mechanics, but now I also think these little flies also illustrate something interesting (or maybe just confusing) about the putative benefits of a sexual lifestyle (one of the major hypotheses for why bacteria are naturally competent).

There are three kinds of chromosomes in fungus gnats, each of which behaves in an unusual way compared to familiar eukaryotic transmission genetics. In this post, I’ll focus on the autosomes, which illustrate how tangled and confusing the issues can become when thinking about the evolution of sex.*

In fungus gnats, males only transmit their mother’s autosomes! That’s right: The males are diploid, obtaining a complement of autosomes from mom and a complement from dad. But somehow, their sperm only include maternal autosomal chromosomes. (Females transmit their autosomes in the ordinary fashion.) From a chromosome dynamics and epigenetics standpoint, this is a very interesting germline development and meiosis** (and offers some entertaining genetics thought-experiments), but what about with respect to the evolution of sex?

Fungus gnats aren’t the only group of animals where males only transmit their maternal autosomes; it’s also true in haplo-diploid hymenopterans, like honey bees. In these animals, males arise from unfertilized eggs (sometimes called arrhenotoky), so that male honey bees are typically haploid. Thus the sperm these males make is also non-recombinant (by necessity, since there’s no homolog there at all) and contain only maternal genetic material.

Why is this of interest? I personally often get confused when reading even simplistic writings on the evolution (or maintenance) of sex. Part of the problem is that numerous issues are often entangled, in this case the issue of ploidy and several overlaying issues of recombination. So describing this unusual lifestyle is not meant to simplify things, but rather to point out just how difficult it can be to think about why an organism might adopt a particular lifestyle.

I’ll talk more extensively about the (simpler) theoretical reasons why sex is thought to be advantageous in another post, but for now the one really major reason that’s always cropping up is that sex offers the chance to recombine two different genotypes to produce new combinations of alleles in the next generation. So sexual recombination, or generating haplotypic diversity, is often considered a major force that maintains a sexual lifestyle.

This is all fine and good, but there appear to be numerous instances of sexual lifestyles that have ameliorated-- but not eliminated-- recombination, raising a variety of questions. A good example of this is the absence of recombination between autosomes in drosophila (fruit fly) males. For a given autosome, a male fruit fly will transmit to his offspring either his mother’s chromosome (which will be recombinant with respect to his maternal grandparents) or his father’s chromosome (which will be non-recombinant with respect to his paternal grandparents). So all else being equal, linkage disequilibrium will break down more slowly in such a population where one sex doesn’t undergo crossing over, as opposed to one where both sexes do.

Genetic transmission is a bit different from this for the fruit fly sex chromosome, the fungus gnat sex chromosomes and autosomes, and all the chromosomes in a honey bee. So for sex chromosomes, since males in all three groups get only a single X from their mother, it will be recombinant with respect to their maternal grandparents but transmitted intact to a male’s progeny. And for the autosomes of both fungus gnats and honey bees, the same thing is true.

But with fungus gnats, males adopt a diploid state, but still behave like a bee with respect to transmitting their autosomes. What’s going on here? One common explanation for the alternation of generations and the haplodiploid lifestyles (i.e. keeping separate haploid and diploid states) is that haploids and diploids feel the effects of natural selection differently. While a recessive allele in a diploid population only manifests when the allele is homozygous, it is always exposed in a haploid. So selection acts more quickly on haploids, and greater allelic diversity (and slower selection) can exist in diploid populations. By having both states in a population, the benefits of both can be enjoyed.

Okay, so that’s all pretty confusing, but I think the take-home is this (all else being equal, except ploidy and genetic transmission mechanism):
(1) Fungus gnat males usually get to cover their recessive alleles by being diploid-- as with fruit flies. But honey bee populations feel selection much more strongly, since their recessive mutations are always uncovered by another allele in males. So deleterious alleles can presumably be weeded out more efficiently in the honey bee than the other two, while recessive alleles have more of a chance to lurk in the fly populations.
(2) But on the other hand (all else being equal) linkage disequilibrium would presumably break down more quickly in fungus gnats and honey bees than in fruit flies, though not as quickly as if homologous pairs recombined in both sexes meiosis.

So there seems to be numerous forces balancing each other here. At a minimum, even ignoring the rest of the factors, the way alleles and combinations of alleles will behave over generations in these three animals will be distinct, depending on the mode of genetic transmission and the ploidy in the different males. The only thing that (all else being equal) is the same between all three animals is the sex chromosome. So the fungus gnat lifestyle offers an interesting hedged strategy as compared to the more familiar fruit fly and bee lifestyles, as well as having some very compelling chromosome mechanics.

* I’ll mention the other two types of chromosomes, just to illustrate how much interesting stuff is going on here: (1) The sex chromosome (X) always non-disjoins in meiosis II in males, such that every sperm is disomic for the X chromosome and thus every zygote is trisomic for the X. Later in development, the elimination of 1 or 2 X chromosomes determines the sex of the animal (female or male, respectively). (2) The limited chromosomes (L) are small heterochromatic knob chromosomes that are only present in the germline, and are somehow eliminated from somatic tissues by selective non-disjunction. So those are two very interesting phenomena in sciarids that will hopefully deserve future mention...

** How do the males accomplish this featof maternal-only autosome transmission? First of all, like many other male dipterans, there is no crossing over between homologous chromosomes. This is also the case in the model organism Drosophila melanogaster. Second, somehow only the maternal autosomes form kinetochores at their centromeres in the meiosis I division, so the paternal autosomes get left behind by the unusual asymmetric spindle of the male meiosis. This means that throughout the germline mitotic divisions, something distinguishes the maternal from paternal chromosomes that then manifests in the first meiotic division...


  1. Fungus gnats are those tiny black flies that breed in the soil of houseplants whose soil surface is kept moist. (Learned through experience.)

  2. I need to learn to be more succinct!

  3. This is facinating Chang! I've got questions for you!! If fungus gnat larvae were parasites of mammals (lets imagine) combined with the rare reproductive state of paedogenesis which is evident with these dipterans - ie the larvae, not adults, produce live young but in doing so, the larva is killed in the process.
    What would the males being diploid mean? Would it have any bearing on the above? many thanks Jo

  4. Hi Jo!

    Pretty much everything I know about Sciara, I learned in the seminal text "Animal Cytology and Evolution", by MJD White. I love that book. The third edition is the one I've worked on reading through.

    I'm not sure how parasitism would play into this, and paedogenesis would probably only matter if only one sex killed its mom during child-birth, but shouldn't make much difference otherwise.

    Do you work on a paedogenetic parasite, per chance?

  5. Thanks Chang!

    So it may not make any difference.

    My colleagues and I have got a theory that some fungus gnats have become parasites of vertebrate, causing 'micro-myiasis'. The current name of one of the target diseases is 'Morgellons', with unknown aeitology. Sounds wacky, but I'm very serious - we've started collecting some great evidence. Here's our initial suggestion: http://www.morgellonsuk.org.uk/micromyiasis.htm

    I'm wondering when fungus gnats are due to have their genome mapped?

    I've read that the fungus gnat Bradysia coprophila has this unique genetic system you speak of: males eliminate the entire paternal genome when making sperm, the sex of embryos is determined by X chromosome elimination, chromosomes are eliminated in the formation of the germ-line of both sexes, and in the differentiation of the germ-line and the soma.. Furthermore, the behavior of the X chromosome in male meiosis is mediated by a short stretch of DNA which is not part of a gene...! er?

    How would their unique genetic system affect their evolution, or their development of resistance to pesticides?

    We know that some species have turned to a carnivorous diet (species Orfelia fultoni).

  6. Hiya Jo!

    Wow, your summary of Bradysia coprophila is a far more succinct description of that bizarre lifestyle. I think this is the example I've read about too. Not sure about the bit about the gene/not gene. That's sometimes a dubious distinction anyways. Is a centromere a gene?

    There's very little in the way of modern literature on the subject, though I recall seeing some nice cytogenetics from a Spanish group and a South American group at some point.

    And you and your colleagues ideas about micro-myiasis are interesting. And while bizarre, it seems believable.

    It seems true that some organisms don't get the kind of attention they probably deserve due to, er, unpleasantness. I mean, working on something that is straight out of Alien is possibly unpleasant. And something with a species name like "coprophila" isn't likely to draw a lot of people either.

    Nevertheless, it would be interesting to know whether the fungus gnats you are interested in have the bizarre genetics of Bradysia. It would require the ability to maintain lab colonies of your organism and some basic molecular marker analysis, and it should be pretty straightforward to determine.

    I've no idea if/when any Sciarids will be sequenced, but getting a modern verification of their transmission genetics would probably help it seem more interesting...

    As to how such a genetic system would affect their evolution... I don't really know. Males would respond to selection more slowly than male bees (for autosomal genes). But the breakdown of LD might progress similarly to bees. If there's a why to it all is anyones guess.

  7. I have fungal gnat Myiasis here in NJ USA and it's so rare as you know that the ER at the hospital accused me of self mutilation. Previously I was tring to get the larvae out with a few different methods. Tweezers. Bee sting kit. Suffocation by Vaseline. None really worked. I am immuno compromised and I have leaks in my pipes. We also have a huge crack in condo foundation and you can see the gnats pasted to the siding.

    Plumbing Getting fixed Monday. I have the kind where they go for previously wounded skin. Scars from a biopsy on leg, scars on calf from shaving incident when I was young, where I recently had shingles (back, neck). Started with scalp. Read on web that woman shaved her head as they go for the roots. Well stupid me went and shaved nearly my entire body. I suppose the second time I used razor it was contaminated so I also have this on my left arm. That's the one I picked at as it was big. Coincidentally I had a hookworm scar from where one entered years ago either while on vacation or cleaning feral cat's litter box. Ever since I thought I still had it. It wasn't self limiting for me as I have trouble swallowing (Sjogrens Syndrome) and eventually I had funky sinuses and bad bathroom episodes (episodes??? Lol) and I couldn't get a proper diagnosis here in the states. Since I have 2 Autoimune diseases it's hard or me to muster up energy for much.

    Anyway today I am using Ivermectin I ordered online legally for horses. I am using it topically and it's working great on the big wound I picked at. I honestly think there's a monster in there. If I had my bee sting kit is try that after I soften the shanks (is that what they're called? ) because shanks are PAINFUL to remove. This thing won't come out by itself. Too deep to not keep covered. Once in a while spits out little white baby larvae (excuse my mom science background) and makes new sores!! Even under darned bandage!

    Am I so rare to have this? I'm not diagnosed but I've got preserved samples, pictures and lots of xanax because at first I was panicked 24/7. Now I know I'll get over it I just gotta get the big one out. If anyone wants to know more my e m a i l is carolhop at optonline dot net

    So now I have from hospital a prescription for an antibiotic (keflex) and a "sentence " (haha ) to Intensive Outpatient a Therapy for 6 weeks. ER doctor was truly ignorant and did not live up to his oath

  8. PS I forgot to add a question: would the fungal gnats go for any hookworms disseminated thru out my body? The antibiotic and or gnats or pupa? Seemed to eliminate a lot of my hookworms

    1. Im in ny and i think i have the same problem. Did you ever heal ?

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