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.

           

Barriers to work in retirement

My experience at wishing to remain active as a scientist after retiring for Newcastle University has not been an unalloyed joy. On the positive side there is a scheme by Leverhulme Trust to finance original research by retired university staff. This is an excellent initiative but my interest is now in tying up loose ends from my years of active research rather than in original research. In attempting to achieve this I have encountered a number of barriers.

For example, access to the scientific literature through the Athens web sight is cut off at retirement. Furthermore, I am beginning to suspect that some universities in the UK have a 'spam filter' installed on e-mail that excludes messages that do not originate from another university i.e. with e-male address ending in 'ac.uk'. I hope I am wrong about this but it would explain a lot of the difficulties I am experiencing in communicating with academic colleagues. 

There is more. The new open access journals that are spring up everywhere (Nature Editorial 2012, Van Noorden 2012), offer a quick and easy way of publishing which suits me very well just now. But the costs of open access publication fall to the author rather than the readers. These costs are typically substantial, up to c.£500.00 per paper. Publishers expect university libraries to help authors with these costs but, at least in the case of Newcastle University’s Robinson library this does not happen. The result is that authors on slender academic pensions must pay the cost of publication. The problem is succinctly put by Christopher Smith (2012) and pungently by Jeffrey Beall (2012). I have just come across an encouraging change in this with a move to offer authors a lifetime’s free publication after the paying of a small fee (Van Noorden 2012). What good news.

There is no help in attending conferences. Costs, including registration fees, travel and accommodation are prohibitive. I would have liked to travel to Sweden for the 2012 meeting of the International Society for Behavioural Ecology. Before retirement these costs would be born by the home university or would be included in a research grant.

Because of all this, and after publishing two major reviews in a conventional journal and four smaller ones in open access journals, I have virtually given up attempting to publish and turned instead to Blogging. If my experience is a common one, it seems to me that the scientific enterprise is excluding its most experienced scientists. We will all be losers unless this issue is confronted.

References

Nature Editorial (1012). Openness costs. Nature, 486, 439.

Beall, J. (2012). Predatory publishers are corrupting open access. Nature, 489. 179.

Smith, C. (2012). Open access: hard on lone authors. Nature, 487, 432.

Van Noorden, R. (2012). "Britain Aims for Broad Open Access." Nature 486: 302-303.

           

Van Noorden, R. (2012). "Journal Offers flat Fee for  'all you can publish'." Nature 486: 166.

           

Fungal gardens, the rumen and the rectum

The complex stomach of ruminants is well known. It is designed by natural selection to provide a habitat for decomposer micro-organisms that possess the metabolic machinery to process the high cellulose food eaten by the ruminant. Ruminants cannot do this for themselves. The nourishment obtained by the ruminant comes principally from the digestion of the micro-organisms and their metabolites rather than form the grass itself.

The external rumen (Swift et al.1979), works in exactly the same way but the decomposers are active outside the animal’s body. This concept has been central to much of my work on the larval stages of aquatic insects (see McLachlan and Ladle 2009 for review). The principal source of food for these animals, just like for ruminants, is composed largely of cellulose in the form of dead organic matter (detritus).

Changes in the micro-organisms associated with detritus (peat) in a bog lake. (a) Peat from moor land before entering the lake. (B) Peat in suspension in lake water following erosion by wave action. Arrows indicate probable bacilli. (C) A faecal pellet of Chironomus lugubris composed of peat particles. (D) Close-up of pellet showing fungal hyphae on the surface. (E) Bacteria associated with a pellet disintegrated by the feeding activities of Chydorus sphaericus. (F) close-up of bacilli in (E). Scale lines A-E, 10μm. F, 1μm. From McLachlan, et al. (1979).

The point I wish to make here follows my reading the Conway Morris’s book (2003). This book has led me to realise that the concept of the external rumen has another quite different application. I refer to the fungal gardens of several species of ants and termites.These highly eusocial insects plant and tend the fungal gardens in adaptive convergence on human agriculture. The gardens are supplied with indigestible detritus by these insects but the fungus which grows on it is nutritious and appears to be the sole food of the ants. The parallel to the external rumen of aquatic detritivores is striking. 

Humans too are composed of a multitude of genomes (Blaser 2011). Indeed, whole genome sequencing techniques have lead to the realisation that the human genome includes the genes of micro-organisms dwelling largely in the rectum (Lupp,C. et al. 2012. Relman 2012). Is ther any connection here to the biblical quote...“…what is your name and he answered “Legion” for many demons had entered him (Luke 8:3). 

References

Blaser, M. (2011). "Stop the killing of beneficial bacteria." Nature 476: 393, 394.

Conway Morris, S. (2003). Life’s Solution: Inevitable Humans in a Lonely Universe. Cambridge University Press, Cambridge, UK.

Lupp, C., Skipper, M., Weiss, U. (2012). Gut microbes and health. Nature 489: 219.

McLachlan, A. J., Pearce, L. J. and Smith, J. A. (1989. Feeding interactions and cycling of peat in a bog lake. Journal of Animal Ecology 48, 850-861.  (1979).

McLachlan, A. J. and Ladle, R. J. (2009). The evolutionary ecology of detritus feeding in the larvae of freshwater Diptera. Biological Reviews, 84, 133-141.

Relman, D. A. (2012). Learning about who we are. Nature, 486, 194.

Swift, M. J., M. J. , Heal, O. W. and Anderson, J. M. (1979). Decomposition in Terrestrial Ecosystems. Blackwell, London.

Swarm Based Mating Systems

For many years I have been grappling with the elusive mating system of the common chironomid midge. This effort has been based, at least in part, on observations of swarms in the wild. The swarm is essentially a lek with aggregations of males, often numbering many thousand individuals, keeping station over a landmark to attract patrolling females. Females enter the swarm and emerge after a short time with a mate (Downes 1969; McLachlan and Neems 1995). Mosquitoes share this mating system with chironomids and others and more than 200 years ago, Hiram Maxwell, the inventor to the machine-gun showed, in a series of careful observations on mosquitoes, that paring within the swarm hinges on the sound emitted by the wing-beat of the individuals of both sexes, cited by (Roth, Roth et al. 1966). I had lost sight of Maxwell’s work but recently rediscovered the role of sound in swarm based mating systems in a rich literature (Stumpner and van Heelversin 2001; Bailey 2003). Like that of Maxwell, this work principally concerns disease carrying mosquitoes and it has been known for many years that it is the Johnston’s organ at the base of the antenna that responds to vibrations set up in the antenna itself (Johnston, C. 1855).

I had previously concluded (McLachlan 2011) p3, para 4, as follows: …”wing beat sound, I suggest, is a fallible cue..”. This conclusion skirts close to the answer but misses the point, elegantly demonstrated by Gabriella Gibson and others (Ng'Habi, Huho et al. 2008; Cator, Arthur et al. 2009; Cator, Ng'habi et al. 2010; Gibson, Warren et al. 2010), that wing beat sound varies because individuals of both sexes are searching for harmonics, which if achieved, signals the presence of a suitable mate. Wing beat sound is related to body size (Cator, Ng'habi et al. 2010), and body size in turn generally reflects genetical quality in animals (Krebs and Davies 1981), thus facilitating mate choice within a sexual selection landscape. It is difficult to escape the conclusion that among swarm based mating systems, it is not the female that chooses a mate, as is the common situation in leks (Andersson 1994). Nor does the male make the choice (Andersson 1994; Clutton-Brock 2009). Rather, both sexes appear equally responsible for choice. It seems likely that mutual mate choice is typical of swarm based mating systems and even more generally among tiny animals such as the insects where finding a mate might be the major selective pressure leading to the evolution of this mating system. Mutual mate choice seen in a very different of insect, the fire-fly (a beetle) (Thornhill and Alcock 1983), pp156-159, lends credence to this conjecture. The speed with which a mating can be achieved in the face of danger from predators (Moller, Christiansen et al. 2011), such as empids could be a contributing factor.

Read in the context of (McLachlan and Neems 1995; McLachlan 2011), all the steps leading to mating within such leks fall into place at last. First there is the gathering of males over landmarks using both visual and auditory cues, the latter involving the elaborate antennae of the male. Next, the male swarm is located by patrolling females, again using both visual and auditory cues. The female antenna is less elaborate but is presumably sufficiently sensitive to detect the sound emitted by a large aggregation of males. Finally, both sexes deliberately vary wing beat frequency searching for harmonics which lead to mating.

These conclusions call into question my earlier suggestion that the mating system is essentially driven by sexual coercion, with aggressive males pursuing fleeing females (McLachlan, Pike et al. 2008) p.267 para.2 and (McLachlan 2011), Conclusions lines 5,6. If coercion is not part of the story, how exactly is pairing achieved? I suggest that the male is the active part of a pairing event with his superior antennae and greater agility (McLachlan 1986; McLachlan, Pike et al. 2008), but that the female does not flee. Rather she offers herself and awaits capture. Therefore, in the light of the evidence currently available, I reluctantly abandon the idea of a mating system driven by coercion. It seemed to explain so much (McLachlan, Pike et al. 2008), p267, but is not good enough. This change in emphasis has no baring on understanding the role of the key predator of male midges, the empid fly (McLachlan, Ladle et al. 2003). It is worth noting though, that by contrast with the performance of the male midge in capturing mates, this predator, possible operating entirely on sight, has a dismal performance. But, since male midges are so plentiful, the empid may not need to be any more efficient.

Some further comment is required on the term ‘choice’. This term is central to sexual selection theory but is an anthropomorphism which worries some biologists. Here I sidestep this concern by adopting the attitude of West-Eberhard (West-Eberhard 2003) pp34 – 35), where choice is defined as taking place when ... “an organism responds differentially to different stimuli”.

References

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

Bailey, W. J. (2003). "Insect duets: Underlying Mechanisms and their Evolution." Physiological Entomology 28: 157-174.

Cator, L. J., B. J. Arthur, et al. (2009). "Harmonic Convergence in the Love Songs of the Denque Vector Mosquito." Science 323: 1077-1079.

Cator, L. J., K. R. Ng'habi, et al. (2010). "Sizing up a mate: variation in production and response to acoustic signals in Anopheles gambiae." Behavioural Ecology 21: 1033-1039.

Clutton-Brock, T. (2009). "Sexual Selection in Females." Animal Behaviour 77: 3-11.

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

Gibson, G., B. Warren, et al. (2010). "Humming in Tune: Sex and Species Recognition by Mosquitoes on the Wing." Journal of the Association for Research in Otolaryngology. 11: 527-540.

Jonaston, C. (1855). "Auditory apparatus of the Culex mosquito". Quarterly Journal of Microscopic Science. 3, 97-102.

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

McLachlan, A. J. (1986). "Sexual dimorphism in midges: strategies for flight in the rain-pool dweller Chironomus imicola (Diptera: Chironomidae)." Journal of Animal Ecology 55: 261-267.

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., 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.

McLachlan, A. J., T. W. Pike, et al. (2008). "Another kind of symmetry: are there adaptive benefits to the arrangement of mites on an insect host?" Ethology Ecology & Evolution 20: 257-270.

Moller, A. P., S. Christiansen, et al. (2011). "Sexual signals, risk of predation and escape behaviour." Behavioural Ecology doi:10.1093/beheco/arr046: 800-807.

Ng'Habi, K. R., B. J. Huho, et al. (2008). "Sexual Selection in Mosquito Swarms: May the Best Man Lose?

." Animal Behaviour 76: 105-112.

Roth, M., L. M. Roth, et al. (1966). "The allure of the female mosquito." Natural History 75: 27.

Stumpner, A. and D. van Heelversin (2001). "Evolution and Function of Auditory Systems in Insects. ." Naturwissenshaften 88: 159-170.

Thornhill, R. and J. Alcock (1983). The Evolution of Insect Mating Systems. London, Harvard University Press.

West-Eberhard, M. J. (2003). Developmental Plasticity and Evolution. Oxford, Oxford University Press.