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...