Anhydrobiosis, parasites and sex.

I have been reading Hayden’s article (Hayden 2008), which discusses the possibility that bdelloid rotifers have dispensed with sex entirely. If they have done so, and the evidence is good that they have (Flot, Hespeels et al. 2013), it would be an extraordinary and perhaps unique case among metazoa. It has been proposed (Ridley 1993), quoting Richard Ladle in interview, that the absence of sex can evolve only among animals able to dry out, called anhydrobiosis or cryptobiosis, because desiccation eliminates parasites. It follows that sex may have evolved to combat parasites (Hamilton and Zuk 1982). The ability to withstand desiccation is a widespread adaptation to unpredictable periodic drought. It is found, at some stage of the life-cycle, in organisms from bacteria to fish and is often linked to reproduction in the absence of sex (parthenogenesis). Thus the link between parthenogenesis and anhydrobiosis is of fundamental interest to the role of parasites and the functions and origin of sex (Maynard Smith 1978).

Sharing rain pools in the tropics with huge populations of the bdelloid rotifer Philodina roseola is another organism capable of anhydrobiosis. I refer to the insect Polypedilum vanderplanki (Hinton 1951), also present in huge numbers. Aquatic larval stage of this species inhabit rain pools and are capable of surviving desiccation of their home pool by loosing almost all tissue water and entering a state of suspended animation. P. vanderplanki larvae are the most complex organism to have evolved the trick of anhydrobiosis beyond the egg stage. Adult Polypedilum vanderplanki look just like any other chironomid midge with normal males and females. A test for the presence of parthenogenesis is the absence of males in a population, but note that the presence of both sexes does not alone exclude the possibility of periodic parthenogenesis. There are some 15,000 species of chironomid worldwide (Armitage, Cranston et al. 1995), yet as far as it is known, among all these larvae, Polypedilum vanderplanki is alone able to survive desiccation. Incidentally, a worthwhile project would be to carry out a phylogenetic analysis of the 36 African Polypedilum species listed by Freeman (Freeman 1955), to determine where the apparently unique ability of P.vanderplanki came from (but see also my blog Life Cycle Adaptations among chironomid midges. Testing the hypotheses). Larvae have been shown to survive almost total desiccation for many years in the laboratory (Hinton 1968). A drop of water leads to prompt recover with larvae taking up their busy lives where they left of, potentially many years before.

It seems to me that Polypedilum vanderplanki would provide a good organism with which to test the presumed association of anhydrobiosis and sex in Philodina roseola and other bdelloids.  For example, both Polypedilum and Philodina occupy the same unpredictable habitat and both share anhydrobiosis. The obvious test is to ask how Polypedilum vanderplanki compares to Philodina roseola in two regards. First, does Polypedilum vanderplanki engage exclusively in normal sex seen in most other chironomids and if so, why? Should there not be a fitness advantage to the loss of sex here too? Given time the loss of sex could presumably be achieved b adaptive evolution in P. vanderplanki too.  Second, does P.vanderplanki enjoy the absence of parasites in the life cycle? Both are testable hypotheses, in principal, and might help resolve some knotty difficulties. An experiment to test for the presence of parasites can readily be imagined with the experimental treatment involving the collection of adult P.vanderplanki emerging from pools in the wild. Collection can realistically be achieved by placing a screened tent over selected pools to trap emerging adults. A suitable control treatment could involve the collection, by the same tent method, of chironimid species inhabiting 'permanent' waters. For example, it would be instructive to test  Polypedilum species inhabiting 'permanent' waters. Common parasites of chironomid adults include mites of the genus Unionicola and the nematode worm Gastromermis rosea (McLachlan, A. J. 2006). Both are easily seen on or in adult midges.   

A caveat to the picture developed above emerges for the efforts of two authors working with bdelloid rotifers inhabiting very transient wet habitats such as moss and the bark of trees (Wilson and Sherman 2013). They show that anhydrobiosis is aided in the escape from co-evolving parasites by the ability to disperse in the dehydrated state, thus leaving parasites behind. Can P.vanderplanki disperse as a desiccated larva?   Recall the early suggestion by Charles Darwin (Darwin 1859), and more recently by Frisch et al (Frisch, Green et al. 2007), among others, that aquatic organs can disperse by chance on the feet of aquatic birds. It therefore seems probably that dispersal as a dry larva is open to P.vanderplanki. But P.vanderplanki has an additional method of dispersal – by means of the flying adult. An adult emerging from a putative disease-free larva is presumably also disease free. Thus P. vanderplanki may be regarded as well equipped to avoid disease. 

The answer to the puzzle of the retention of sex in P.vanderplanki may lie in an unexpected place. A recent conversation with Roger Butlin made me aware of the  large body of work by Meselson and collaborators concerning the genetics of Bdelloid rotifers (Gladyshev, M. et al. 2008) .They show that these rotifers are able to obtain genes direct for the aquatic environment without the intervention of parasites or sex. To explain: sex is thought to play an essential role in maintaining genetic diversity (Maynard Smith 1978). In the absence of sex, horizontal gene transfer, well know among the bacteria, can achieve the same end. For the metazoa, horizontal gene transfer is achieved with the aid of the parasites, particularly the viruses (Boto 2010). But I have just made the case for the absence of parasites in organisms capable of anhydrobiosis. It is here that Bdelloid rotifers come in to provide an example of horizontal gene transfer among metazoa, evidently in the absence of parasites, thus obviating the need for sex. The persistence of sex in P. vanderplanki may thus be explained by the absence of the extraordinary trick of the rotifers, that is, the ability to sample genes from the surrounding water. Perhaps the abiliy to sample genes from the water of a rein pool will eventually evolve in P. vanderplanki larvae as well.   

References

Armitage, P., P. S. Cranston, et al. (1995). The Chironomidae. The biology and ecology of non -biting midges. . London, Chapman & Hall.

           

Boto, L. (2010). "Horizontal Gene Transfer in Evolution: facts and challenges." Proceedings of the Royal Society (B) 277: 819-827.

           

Darwin, C. (1859). The origin of species by means of natural selection, or the preservation of favoured races in the struggle of life. London, John Murray.

           

Flot, J.-F., B. Hespeels, et al. (2013). "Genomic evidence for amniotic evolution in the bdelloid rotifer Adineta vaga." Nature 500: 453-457.

           

Freeman, P. (1955). "A study of the Chironomidae (Diptera) of Africa South of the Sahara. ." The Bulletin of the British Museum (Natural History) 4: 1-69.

           

Frisch, D., A. J. Green, et al. (2007). "High dispersal capacity of a broad specturm of aquatic invertebrates via waterbirds." Aquatic Science 69: 568-574.

           

Gladyshev, E. A., M. M., et al. (2008). "Massive Horizontal Gene Transfer in bdelloid Rotifers." Science 320: 1210-1213.

           

Hamilton, W. D. and M. Zuk (1982). "Heritable true fitness and bright birds: a role for parasites?

:." Science 218: 384-387.

           

Hayden, E. C. (2008). "Scandal! Sex starved and still surviving. ." Nature 452: 678-680.

           

Hinton, H. E. (1951). "A new chironomid from Africa." Proceedings of the Zoological Society of London. 121: 371-380.

           

Hinton, H. E. (1968). "Reversible suspension of metabolism and the origin of life. ." Proceedings of the Royal Society, London (B). 171: 43-47.

           

Maynard Smith, J. (1978). The Evolution of Sex. Cambridge, UK, Cambridge University Press.

McLachlan, A. J. (2006). You are looking mitey fine: parasite a direct indicators of fitness in the mating system of a host species. Ethology Ecology & Evolution, 18. 233-239.

           

Ridley, M. (1993). The Red Queen. Sex and the Evolution of Human Nature. Harmandsworth, UK, Penguine Books.

           

Wilson, C. G. and P. W. Sherman (2013). "Spatial and temporal escape from fungal parasites in natural communities of ancient asexual bdelloid rotifers." Proceedings of the Royal Society (B). 280.