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. 

Further notes on Rain pools

 Here I make some points which I had missed, or failed to emphasise previously (see [1] and Blog 28/12/2010). First, in terms of species composition and by contrast with those on soil [2], rain pools on rock are characterised by high density mono-cultures of  the larvae of indigenous insect species, typically those of  chironomid species.Small habitat patches like these rain pools, seem too small to provide barriers to gene flow upon which speciation commonly depends. The presence of a single species in each pool could therefore have been be predicted. The same is true of the fish populations of some very small lakes in Cameroon which, by contrast to the massive adaptive radiation seen among the cichlid flocks of the larger African lakes, are each inhabited by a single fish species [3], pp 200, 201. Such monocultures are the hallmark of the extreme habitats and are termed extremophiles [4]. Extremophiles provide the focus for exobiology – the search for life elsewhere in the universe. Perhaps, in a sense, parasites could be included here. The reason for this suggeston is that parasites are typically likewise confined to a single host where adaptive evolution has enabled them to circumvent formidable host defences. When occupation of a host is achieved there is no interspecific competition for the rich host resources leading to high density monocultures, ecologically equivalent to the high invertebrate densities of rain pool faunas.

Second, in terms of duration, rain pools on rock can useful to compare cecidomyian gall midges inhabiting mushrooms. Like rain pools mushroom provide a transient habitat because they are consumed by the inhabitants. The strange adaptive consequences are described by Gould [5], p93. I do not detail them here but it is worth reading Gould's account for its heuristic value. 

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

2.         Williams, D.D., The Biology of Temporary Waters. 2006, Oxford: Oxford University Press.

3.         Coyne, J. A. (2009). Why Evolution is true. Oxford University Press, UK.
4.         Nee, S., Introducing the extremophiles. Vol. 448. 2007, London: Nature.
5.         Gould, S, J. (1980). Organic Wisdom. Or Why Should a Fly Eat its Mother From Inside. In: Ever Since Darwin. Reflections in Natural History. Penguine Books. 

Biting Midges

I want to make two points about the mating system of biting midges (Culicoides), as subjects for comparative work with non-biting midges (Chironomidae). First, the biting midges are very small flies which introduce interesting biomechanical questions about flight in the mating arena. Second, females of biting midges are readily collected from swarms. Chironomid females do not aggregate like this and are therefore difficult to collect. These differences provides the opportunity to resolve some long standing questions about the mating system of these flies. Here I adopt the ubiquitous Chironomus plumosus as test species for the non-biters and the dreaded Scottish midge, Culicoides impunctatus, for the biters.   

Biomechanical aspect of flight

Chironomus plumosus has a wing length of c. 4.4mm in the female while for Culicoides impunctatus it is c.1.4mm, i.e. about three times smaller than Chironomus. Culicoides is a very small insect indeed, barely visible to the naked eye, hence the name ‘no-see-ums’ in parts of the States. Whereas the size of Chironomus appears to place individuals on the edge of the inertial and viscous universes when in flight (Crompton, Thomason et al. 2003), size would be predicted to place flying Culicoides individuals firmly in a viscous universe (Vogel 1994). Thus comparative work based on size introduces some interesting proximate questions. For example, when in flight Culicoides may encounter air somewhere near the viscosity of treacle.  In attempting a pairing in a mating swarm, how do the sexes of Culicoides manoeuvre under these conditions?

Behaviour of females in mating swarms

The comparative approach here is based on the fact that the mating system of midges and many other swarming Diptera are leks and therefore essentially similar (Downes 1969; McLachlan and Neems 1995; Hendry 2003). Most species in both taxa mate on the wing. These mating systems involve swarms of males that attract females which enter the swarm singly or in small numbers, soon to leave tightly paired with a male. Hence females are scarce in the swarm, i.e. the operational sex ratio is strongly male biased. Crucially, unlike Chironomus, females of Culicoides also form swarms, just like males. Female swarms here are feeding swarms where females search for blood meals. Consequently, Culicoides females are abundant and readily capture. This means that Culicoides females can be used to test hypotheses about the mating system that are very difficult with chironomids.

For example, hypotheses about the central role of female body size in mating success can be tested using Culicoides females. The determination of  body size in both mated and unmated females will help resolve interesting questions such as the role of sexual coercion by males (McLachlan 2011; McLachlan 2012), and of predation on mating swarms by flies such as empids (McLachlan, Ladle et al. 2003). These questions are interconnected with biomechanical effect because larger females are predicted to be slower in flight and hence to be the more readily captured by both males and predacious flies. Captured Culicoides females provide data on unmated females for comparison with those captured emerging from mating swarms paired with males.  However, few biologists have the motivation to voluntarily approach these hellish feeding swarms, so the curiosity driven research opportunities described here are at something of an impasse at present.

I have just read a paper by Tripet et al (2009), which suggests a resolution for one puzzle; i.e. what do the females of biting flies gain by swarming? It is not a part of the mating system so why do they do it? The explanation proposed is that communal feeding may carry fitness benefits for the flies in circumventing the host immune response. The reasoning here is that the host's immune system inhibits biting a by the flies and that the injection of saliva during feeding suppresses this. Thus swarming may be a necessary prerequisite for communal feeding. Not very nice for the host! Tripet's findings apply to sand flies, not biting midges, suggesting that communal feeding may be a widespread adaptation among biting insets for reasons connected with the immune response of the host.

References

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.

Downes, J. A. (1969). "The swarming and mating flight of Diptera." Annual Review of Entomology 14: 171-297.

Hendry, G. (2003). Midges in Scotland. Edinburgh, Mercat Press.

McLachlan, A. J. (2011). "Homosexual Pairing within a Swarm-Based Mating System: The Case of the Chironomid Midge." Psyche ID 854820: 5 pages.

McLachlan, A. J. (2012). "Phenotypic plasticity and adaptation in a holometabolous insect, the chironomid midge." ISRN Zoology, 8 pages.

McLachlan, A. J., R. Ladle, et al. (2003). "Predator-prey interactions on the wing: aerobatics and body size among dance flies and midges." Animal Behaviour 66: 911-915.

McLachlan, A. J. and R. M. Neems (1995). Swarm based mating systems. Insect Reproduction. S. R. Leather and J. Hardie. New York, CRC Press.
Tripet, F., Cleg, S., Elnaiem, D. E. and Ward, R. D. (2009). Cooperative blood feeding and the function and implications of feeding aggregations in the sand fly, Lutzomyia longipalpis (Diptera: Psychodidae). PLoS Negl. Trop. Dis. 3, e503. 

Vogel, S. (1994). Life in moving fluids. Princeton, Princeton University Press.

Arms Races, Co-Evolution and the Balance of Nature

Two things have prompted me to write some notes on these related topics. First, there are the flaws I see in the concept of the ecosystem as composed of co-evolved entities closely locked together in an arms race. Second, there is the bizarre view that the media have of nature. This is shocking since, in the case of the TV Documentaries series, I understood that their remit was public education.

An evolutionary arms race involves one or more organisms engaged in competition, each being driven by natural selection to out-adapt to the other. Good examples are the competition between predator and prey or between parasite and host  (Dawkins 1986). Each adaptation demands a reciprocal adaptation from the other, much like the arms race between tanks and anti-tank weapons. Arms races never end. To be adapted organism must constantly change. This realisation evokes the Red Queen (Carroll 1865). In the world of the Red Queen just to stay in the same place requires constant running (Van Valen 1973).There are very specific requirements for arms races in the natural world. An evolutionary arms race can only get going between living organisms and cannot involve non-living things because these cannot respond to natural selection. This is my difficulty with the concept of the ecosystem and, incidentally, with the concept of niche construction (Odling-Smee et al 2003). The ecosystem idea requires that arms races involve both living and non-living components, the latter comprising things like nest construction but also bi-products of activity such as urine and CO₂ and O₂. A limited case might be made for the former,  see (Dawkins 2004), but I fail to see how organisms and their urine, mixed with that of others, can co-evolve. Thus the view of ecosystems composed of co-evolved organisms and environment closely locked together by natural selection is deeply flawed, e.g. (Marris 2005; Marris 2009). Even in the living part of an ecosystem, species are continually invading and leaving so that any community is typically in flux (Belovsky, Botkin et al. 2004) pp.348, 349. paragraph 60. Viewing an ecosystem as composed of co-evolved species is the cause of much confusion. For this reason Richard Ladle and I suggest that the ecosystem concept be abandoned (McLachlan and Ladle 2011) p546, paragraph 2. As Dawkins puts it (Dawkins 2004) - a ecosystem is an economy, not a adaptation, so it is pointless expecting over arching co-evolutionary effects there.

This discussion leads me to a widespread fallacy much loved by the media; the idea of the Balance of Nature, which purports that everything in nature is in harmonious balance, beneficial to all (Kircher 2009). Here is an example. On a documentary film clip I viewed recently, an injured giraffe is seen being killed by lions. The explanation of the event is intriguing. It is that nature, by which is presumably meant natural selection, has in its wisdom lead to the death of the giraffe to spare it a long period of suffering. Thus both lions and giraffes benefit. Giving in to a weak ‘balance of nature’ explanation seen here diverts attention from the profound insight that can come only from a proper understanding of the arms race between lions and giraffes. The ‘balance of nature idea’ is flawed because that is not how arms races work, for reviews see (Ridley 1993), pp65-68. (Dawkins 2009), p382-390. (Dawkins 1999), p236-237. Arms races are driven by natural selection which is an impersonal force and cares not a jot for the suffering of the giraffe or any other animal, including man.

References

 Belovsky, G. E., D. B. Botkin, et al. (2004). "Ten Suggestions to Strengthen the Science of Ecology." Bioscience 54: 345-351.

         

Carroll, L. (1865). Alice's Adventures in Wonderland. London, J. M. Dent &Sons Ltd.

           

Dawkins, R. (1986). The Blind Watchmaker. Harlow, UK, Longman Scientific & Technical.

Dawkins, R. (1999). The Extended Phenotype. Oxford University Press, Second Edition.

           
Dawkins, R. (2004). A devil's chaplain. London, Phoenix.

           

Dawkins, R. (2004). "Extended Phenotype - but not too extended. A Reply to Laland, Turner and Jablonka." Biology and Philosophy 19: 377-396.

           

Dawkins, R. (2009). The Greatest Show on Earth. London, Bantam Press.

           

Kircher, J. (2009). The Ballance of Nature: Ecologies Enduring Myth. Princeton, USA., Princeton University Press.

           

Marris, E. (2005). "Shoot to kill." Nature 438: 272-273.

           

Marris, E. (2009). "The End of Invasion?" Nature 459: 327-328.

           

McLachlan, A. J. and R. Ladle (2011). "Barriers to Adaptive Reasoning in Community Ecology." Biological Reviews 86: 543-548.

Odling-Smee, F. J. , Laland, K. N. and Feldman, M. W. (2003). Princeton University Press. Princeton.  
     

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

           

Van Valen, L. (1973). "A New Evolutionary Law." Evolutionary theory 1: 1-30.