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.

           

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.

           

Sexual selection theory.

There has been a long history of debate on sexual selection culminating in the recent controversy published in Animal Behaviour in 2010, (79, e1-e3). The problem starts, I believe, with Charles Darwin’s definition as…”the advantage which certain individuals have over others ….in exclusive relation to reproduction.”(Darwin 1874), p256. I suggest that it is the term ‘reproduction’ that is the cause of the confusion. To quote, ”…in this view, both sexual selection and natural selection are manifested as differential reproductive success”(Spencer and Masters 1992), p206. Yet sexual and natural selection are often considered to be apposing forces with natural selection improving survival and sexual selection reducing it (Spencer and Masters 1992), pp. 295-296. Redefined as activities in exclusive relation to mating (Krebs and Davies 1981) p183, solves some problems but appears prone to fall into the adaptationist trap (Gould 1987), p. 34,35. By this is meant the erection of convincing but untestable hypotheses about adaptation (Spencer and Masters 1992), pp295,296. Furthermore, by  redefining sexual selection in this way leaves several important topics, such as sperm competition, cryptic female choice, sex ratio and reproductive effort, in an uncertain position. These matters remain unresolved and can lead to practical difficulties. For example, my colleague Marion Petrie and I took different views over what to include under Sexual Selection Theory in my module on Behavioural Ecology. There were consequences for the marking of final year exam papers. I believe the status of sexual selection theory is irresoluable, a conclusion which should be born in mind when framing questions in this area. But opinions voiced in a recent debate published in Animal Behaviour (cited above), question the need for a theory of sexual selection at all. This is not the same as my own, less serious, concerns over what should be included under the title. Incidentally, this old chestnut is notable because it has just been reviewed, in exquisite depth and with flare, by Helena Cronin (1994). Remarkable, with the single exception of David Shuker, none of the protagonists cite her at all. Could it be that they are unaware that, because it has already been done, they are wasting their time? Or, as one contributer suggests, it may be the fault of the journal Animal Behaviour for resurrecting, with nothing new to add, an already exhausted debate. 

But that is still not the end of the matter. I note another special issue published by the journal Animal Behaviour (2020. 164. 217-291), where the same ground is churned over yet again. With twelve authors  this is  interesting stuff but I can find not a single reference to Cronin. To laps in this way a second time in baffling among so many learned people. 

References

Cronin, H. (1994). The Ant and the Peacock. Cambridge University Press.

           

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

           

Gould, S. J. (1987). An Urchin in the Storm. London, Collins Harvill.

           

Krebs, J. R. and N. B. Davies (1981). An Introduction to Behavioural Ecology. London, Blackwell Scientific Publications.

           

Spencer, H. G. and J. C. Masters (1992). Sexual Selection: Contemporary Debates. Keywords in Evolutionary Biology. F. K. E. E, A. Lloyd, Harvard University Press.

           

Externally maintained faunas.

Imagine a situation in which individuals are so scarce that they cannot be detected by ordinary sampling methods. In such a scenario, males and females would presumably encounter difficulties in finding each other in order to mate. This is a problem recognised with the sparse faunas of oceanic islands (MacArthur and Wilson, 1967), where it is assumed that island faunas are maintained by immigration from nearby mainland habitats. These mainland habitats have been dubbed source habitats (Wiens and Rotenberry, 1981). Here I consider the case of habitat islands where the faunas may be maintained externally in this way. I refer to ephemeral rain pools in general and to those on rock surfaces in tropical Africa in particular. In a 1988 paper, I discuss the possibility that the seemingly clear adaptations to the tropical rain pool habitat may be illusory. I made this suggestion because larval populations of the relevant species, the chironomid midges Chironomus pulcher and C. imicola, could theoretically be maintained by ovipositing females travelling from permanent lakes and rivers.

In a hypothetical argument, I reasoned that if permanent waters provide ‘source’ faunas, with pools as ‘sink’ habitats, the interesting question is – where does selection operate to shape adaptations in these rain pool species – in source or sink habitats? I have generally assumed that pool faunas are adapted by selection to meet the stringent requirements of life in a transient pool habitat. This seems a reasonable assumption and there is good circumstantial evidence that it is so (McLachlan and Ladle 2001). But, and here lies the problem, if the bulk of the gene pools for these species is to be found in permanent waters, seeking adaptation to rain pools would be a waste of time.

I now wish to overturn the hypothesis that rain pool faunas are maintained externally. I suggest instead that there is a fundamental difference between oceanic island of Wiens and Rotenberry (1981) and MacArthur and Wilson (1967) on the one hand and transient pools on the other. I make this suggestion for two reasons. First, though I have never observed mating, there is ample evidence from counts of egg masses (McLachlan 1988), that breeding occurs in the rain pools. Second, the low densities proposed for source habitats would presumably make breeding unlikely there because of the difficult of finding mates. So, strong selection for parthenogenesis might be expected in the putative source habitats, the lakes and rivers and would therefore be expected to occur in rain pools. Yet I have never been able to demonstrate parthenogenesis among rain pool species. This finding does not eliminate the possibility of parthenogenesis but does suggest that it is not the routine method of reproduction. Indeed, though parthenogenesis is not unknown among chironomid midges, it appears confined to genera other than Chironomus (Williams 1974). I therefore conclude that the low density putative populations in lakes and river is not a a source habitat for rain pool dwelling chironomids.  So the search for adaptations to the extraordinary rain pool habitat is probably a worthwhile enterprise after all.

References

MacArthur, R. H. and Wilson, E. O. (1967). The Theory of Island Biogeography. Princeton University Press.

McLachlan, A. J. (1988). Refugia and habitat partitioning among midges (Diptera: Chironomidae) in rain pools. Ecological Entomology, 13, 185-193.

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

Wiens, J. A. and Rotenberry, J. T. (1981). Censoring and the evaluation of avian habitat occupancy. Studies in Avian Biology.6, 522-532.  

Williams, D. N. (1974). An infestation by a parthenogenetic chironomid. Water Treatment and Examination. 23, 215-232.

A brief note on rain pools

McLachlan and |Neems (1993). Are females selected against in ephemeral habitats? The case of a holometabolous insect (Chironomus pulcher). Oecologia, 94; 93-96.

This paper would have been better entitled: Asymmetric selection on insects in ephemeral habitats: Are the females of rain-pool breeding midges selected against?

Musical Chairs

Somewhere in the 80’s, at a time of austerity, a thriving Zoology Department at Newcastle University was closed. This came as a great shock to us zoologists. We were a strongly motivated lot in a department with large numbers of high quality students and active research programmes. We also enjoyed the inspired leadership of Robert Clark and John Shaw, eminent scientists both. Someone in management appeared to have blundered leading to relocation of all zoologists to various other departments across the campus. At least we still had jobs which were not always the case following closures. After a brief tumultuous period in a Biology Department, to my horror I found myself in something called Agricultural and Environmental Science (AES). I say to my horror because, ever since my early experience in universities in tropical Africa I have had a strong antipathy for applied science, yet here I was in an agriculture centred department! To explain my negative feelings for applied science: biological work in tropical Africa was dominated in the 60’s by fisheries research. Here the ethos demanded the prohibition of any ideas not leading directly to better fish catches. Such trivialisation of research may be excusable in cash-strapped research institute but is totally unacceptable in a university. In this I follow Baron Noel Annan (Annan 1999). To quote him while he was provost of University College London, “Universities exist to cultivate the intellect. Everything else is secondary”. The attitudes to science in Africa affected me deeply. Though my attitude to applied science is indefensible it is an attitude that stays me to this day.

After some years I was able to get out of AES and into the department of Marine Science and Coastal Management. This made no better sense but it enabled me to work closely with David Golding, another displaced zoologist, who was running the zoology degree. The zoology degree had survived closure of the Zoology Department and was an outstandingly successful degree. Hence working with it  was an excellent experience.

 Throughout the whole post-zoology period I managed to contrive to be ‘sidelined’. This is a term used to describe the action taken against colleagues who will not cooperate. It is intended as a punishment but the outcome was that I could get on with the pursuit of my research and teaching interests without the massive administrative distractions integral to this period. In this connection, I am reminded of the words of a Roman consul over 2000 years ago….” We trained hard…but it seemed that every time we were beginning to form up into teams we would be reorganised. I was to learn later in life that we tend to meet any new situation by reorganising; a wonderful method it can be for creating the illusion of progress while producing confusion inefficiency, and demoralisation”. So, things haven’t changed much. Incidentally, I have just discovered that  E.O.Wilson shares my antipathy for endless committees, I quote..." Avoid department-level administration" (Wilson 2013). So I am in good company. 

Overriding all this was the generosity of the University in allowing me long sabbaticals to pursue a key research interest in tropical Africa. I enjoyed a wonderful and fulfilling time at Newcastle University for 35 years and was privileged to work with some outstanding scientists, both student and colleague.

Annan, N. (1999). The Dons: Mentors, Eccentrics and Geniuses. London, Harper Collins Publishers.
Wilson, E. O. (2013). Letters to a young scientist. Liveright/W.W. Norton.