Life Cycle Adaptations among chironomid midges.

In a conversation Mike Cant the other day, he raised a question about adaptive strategies among chironomid midges that started me thinking. Because they are habitats exceptionally amenable to study, I choose rain pools as the case to think about.

But first some background. My interest here is in rain pools on rock surface in tropical Africa – extraordinary because of the huge population of midge larvae indigenous to those pools. Large monocultures are not the case with rain pools on mud, or even rock, elsewhere in the world. Those in tropical Africa are occupied by one of three midge species, Chironomus imicola, Chironomus pulcher or Polypedilum vanderplanki but exclusively only a single species in any pool. For simplicity I start with just one of  these, C. imicola. The biology of these habitats has recently been reviewed (McLachlan and Ladle 2001).

The hypothesis I wish to test is that life cycle in these midges is adaptively appropriate to the average duration of the home pool after rain. In other words, the hypothesis hinges on the apparent relationship between duration of the aquatic larval stage and body size at metamorphosis. Rain pools are ephemeral and highly unpredictable habitats where, for males early emergence from the aquatic larva before the home pool dries would clearly carry fitness benefits. Conversely, a longer time spent as larvae, though risky because of the danger of desiccation, would appear to carry benefits in terms of stamina in dispersal flight after mating and egg carrying capacity for larger females (Crompton, Thomason et al. 2003).Thus, for both sexes there is a trade-off between fitness in the larval and fitness in the adult stages of the life-cycle.

How would a hypothesis relating time to metamorphosis and habitat duration be tested? A a comparative approach in the sense of Nicholas Davies et al. (Davies, Krebs et al. 2012), would be appropriate. A comparison of larval growth rates, sex and size at metamorphosis of chironomid midges for both permanent and ephemeral waters would, in principle, be readily achieved. In the first instance such work would most effectively focus on a comparison of two rain pool dwellers Chironomus imicola with a second rain pool dweller, Polypedilum vanderplanki. The value of this comparison lies in the facts that both inhabit rain pools on rock surfaces in tropical Africa, but from an adaptive point of view must perceive the habitat very differently. This is because Polypedilum vanderplanki is famously capable of surviving the complete desiccation of its home pool as a larva. By contrast, as explained above, Chironomus imicola must leave as an adult before the home pool dries. Hence P.vanderplanki experiences essentially the same pool habitat as permanent and highly predictable while the opposite is true for Chironomus imicola.

Thus a comparison between C. imicola and P. vanderplanki brings with it several advantages, but work need not be confined to these two species. Chironomid midges inhabit almost every inland water body on earth and there are at least 15,000 species to choose from. So the question becomes a far reaching one about evolution of life-cycle adaptations in the context of habitat predictability, in the sense of Southwood  (Southwood 1966). Phylogenetic analysis following the fine work of Pinceel et al. for the fairy shrimps of  temporary pools would greatly strengthen our understanding of the evolutionary affinities among chironomids in relation to habitat duration (Pinceel, Brendonck et al. 2013).

Under my stated hypothesis I predict that a relationship will be found between life-cycle adaptation and habitat predictability over a large range of species. Explicitly, I expect species such as C. imicola, perceiving their habitat as ephemeral, to show early emergence of males and late emergence for females. Species inhabiting and essentially permanent habitat will, by contrast, show synchronous emergence of the sexes. If his prediction is substantiated there are some interesting consequences for our understanding of the mating behaviour of insects. Many species show protandry, that is the early emergence of males, which, ever since Charles Darwin (Darwin 1874), has been thought of as an adaptation to promote mate choice and is thus central to understanding the evolution of mating systems (Andersson 1994; McLachlan and Neems 1995). But, protandry as an adaptation may be an illusion and instead be only a pleiotropic effect of selection for adaptation to habitat duration (McLachlan 1986). 

In testing the above hypothesis at least one important precaution is necessary. We need to have a good understanding of the biology of test species, notably how each perceives habitat predictability from an adaptive point of view. For example, many species of Chironomus are invaders of newly created waters and soon disappear as better competitor arrive (Morduchai-Boltovskoi 1961). So, because of the social effects of competition, such species presumably perceives the habitat as ephemeral even if it last for thousands or even millions of years as in the case of the great lakes of the world.

Resolving questions about life-cycle adaptation in chironomids would find wide application to the understanding of the evolution of adaptations to habitat duration in general. Included here are the communities of carrion, fallen fruit, dung, water pockets trapped in the axils of leaves, water in the pitchers of pitcher plants and many others.  More profoundly, my hypothesis addresses question about the adaptation of organisms to a single clearly identifiable feature of the habitat, its duration.

References

Andersson, M. (1994). Sexual Selection. Princeton, Princeton University Press.

                 

Crompton, B., J. Thomason, et al. (2003). "Mating in a viscous universe: the race is to the agile, not to the swift." Proceedings of the Royal Society, London (B). 270: 1991-1995.

           

Darwin, C. (1874). The descent of man and selection in relation to sex. New York, 1959, The Modern Library, Random House.

           

Davies, N. B., J. R. Krebs, et al. (2012). An Introduction to Behavioural Ecology. Oxford, Wiley-Blackwell.

           

McLachlan, A. J. (1986). Survival of the smallest: advantages and costs of small size in flying animals. Ecological Entomology 11: 237-240.

           

McLachlan, A. J. and R. Ladle (2001). "Life in the puddle: behavioural and life-cycle adaptations in the Diptera of tropical rain pools." Biological Reviews 76: 377-388.

           

McLachlan, A. J. and R. M. Neems (1995). Swarm based mating systems. Insect Reproduction. S. R. Leather and J. Hardie. New York, CRC Press.

           

Morduchai-Boltovskoi, F. D. (1961). "Die entwicklung der Bodenfauna in den Stauseen der Wolga." Verh. Internat. Verein. Limnol. 14: 647-651.

           

Pinceel, T., L. Brendonck, et al. (2013). "Environnmental change as a driver of diversification in temporary aquatic habitats: does the genetic structure of extant fairy shrimp populations reflect historic aridification?" Freshwater Biology 58: 1556-1572.

           

Southwood, T. R. E. (1966). "Habitat, the templet for ecological strategies?" Animal Ecology 46: 337-365.