I RECENTLY REVIEWED some of the advantages and disadvantages of sexual and asexual reproduction. Sexual reproduction is thought to be chiefly useful in the elimination of negative mutations, while these build up in asexually reproducing lineages. Without some type of genetic recombination it is thought that asexual reproduction will lead eventually to extinction.
The rotifers are a group of tiny protostomes. Their phylogenetic relationships are uncertain, as they fall outside of the major protostome groups Lophotrochozoa (containing the annelid worms and molluscs, among others) and the Ecdysozoans (containing the arthropods and nematodes, among others). They can be seen swimming in freshwater, often along with the comparatively larger crustacean Daphnia. Rotifers are named for the corona, an appendage around the mouth bearing cilia that beat rapidly to carry food into the mouth, and appear almost to be spinning like tiny wheels. You can see the corona in action in the video below, vacuuming material into the mouth. Farther down in the body you can see the pharynx contracting rhythmically, a set of hard jaws called trophi macerate food here. Half-way through the video a goblet-shaped organism is caught in the whirlpool current of the corona in the bottom left of the view; I believe this is a Stentor, a type of ciliate (single-celled eukaryote in the phylum Ciliophora). You can see the rotifer’s startle response (bumped by the Stentor?) at the end, when it contracts its body down.
Most rotifers go through cycles of asexual reproduction followed by sexual reproduction, often with the switch linked to high population densities. However, among the bdelloid rotifers a male has never been spotted, and these rotifers appear to have been managing without sexual reproduction for tens of millions of years. How do they do it?
Since asexual reproduction abolishes recombination of chromosomes, a result of this is the elimination of selection requiring alleles for the same gene on two separate chromosomes to serve the same function. Among the sexually reproducing rotifers alleles for a gene usually differ slightly, but in the bdelloid rotifers these can differ greatly. One group found almost 50% sequence divergence for hsp82, a heat shock protein.
The authors of a recent paper hypothesized that this sequence divergence would lead to a divergence in roles for the former alleles. They chose to examine genes usually involved in desiccation tolerance, and picked the group 3 LEA (late embryogenesis abundant) gene found in plants. This gene is involved in desiccation resistance in plant seeds and in invertebrates and many microorganisms. Indeed, in the rotifer Adineta ricciae they found two similar but distinct sequences on two different chromosomes, thought to be sequence-diverged former alleles. The overall sequence divergence was 13.5%. They named these genes Ar-lea-1A and Ar-lea-1B.
Both genes did respond to desiccation, with their expression (the amount of the gene product made, in this case proteins ArLEA1A and ArLEA1B) increasing by about seven times over 24 hours of drying. However, they behaved very differently in solution. LEA genes are usually disordered in solution and coil up when dried. ARLEA1A behaved normally, going from 29% to 84% α-helical when dried, but ARLEA1B has an α-helical structure in solution that does not change greatly upon drying. The relatively small difference in sequence was enough to introduce significant differences in structure.
This difference in structure leads to a difference in function. LEA proteins usually help protect other proteins from aggregation when they are dried, preserving their structure and function for rehydration. ARLEA1A succeeded in this role, but when citrate synthase was dried down with ARLEA1B aggregation actually increased.
Another role of some antidessication LEA proteins is to protect phospholipid bilayers, which are critical for cell integrity. While ARLEA1A does not interact with phospholipid membranes, ARLEA1B was found to associate with these membranes upon drying. This points to two separate roles for these former alleles. One continues in what was probably the primitive function, protecting proteins from desiccation, while the other has apparently amplified an originally minor role to its key role in protecting phospholipid bilayers.
When the rotifers abandoned sexual reproduction they eliminated recombination between synonymous genes on separate chromosomes. This allowed the roles of alleles on separate chromosomes to diverge. The effect was similar to what would be seen in a whole-genome duplication–a sudden increase in the amount of raw material for natural selection. For the past few tens of millions of years the rotifers have been exploiting this extra genetic material. However, once all of the former alleles have diverged completely rotifers will have reached the limit of these resources. Muller’s ratchet will begin to tighten, and eventually the bdelloid rotifers will become extinct.
Pouchkina-Stantcheva, N. N.; McGee, B. M.; Boschetti, C.; Tolleter, D.; Chakrabortee, S.; Popova, A. V.; Meersman, F.; Macherel, D.; Hincha, D. K.; Tunnacliffe, A. “Functional Divergence of Former Alleles in an Ancient Asexual Intertebrate.” Science 2007, 318, 268-271.