Stephen J. Gould on the Scientific Method

Steven J. Gould is widely considered a modern evolutionary biologist of comparable public stature to Richard Dawkins. I would hold Ontogeny and Phylogeny (Gould 1977), among the half dozen most influential biology books I have read in my zoological career. The compelling poetical language is a great bonus. Yet I am puzzled by his understanding of adaptation spelled out in Wilson’s Ladder (Gould 1987) p34.

He considers the attempt to understand adaptation has failed due to what he calls a Panglossian Adaptationism. These Panglossians, he believes, are engaged in an enterprise to label every trait adaptive, purely as an act of belief. These assertions of adaptation he calls Just So Stories from the famous stories for children by Rudyard Kipling (Kipling 1902). Incidentally, it is strange that Gould appears to miss the point to these stories – they are pure Lamarckism. Something could have been made of this.

But this is a quibble. What is fundamental is his misrepresentation of the nature of scientific research. We all know that scientific research requires a testable hypothesis as a starting point. An assumption of adaptation by so called Panglossians is just such a starting point; it is an hypothesis, not a conclusion. Any hypothesis stands or falls after rigorous testing. This is how the hypothetico-deductive process in science works (Medawar 2006) p12-32. I believe Gould is wilfully misunderstanding the matter. This may be one of his bits of mischief such as the fuss over punctuated equilibria (Eldredge and Gould 1972). And reading John Tyler Bonner today (1 November 2018), I find support for my contention (Bonner 1993), pp61-62.

 I therefore reject Gould’s worries about adaptation. A much better appraisal of the difficulties involved in a proper understanding and identification of adaptation is given by George Williams encapsulated in the term teleonomy (Williams 1966).

References

Bonner, J. T. (1993). Life Cycles. Reflection of an Evolutionary Biologist. Princeon Univesity Press.

Eldredge, N. and S. J. Gould (1972). Punctuated Equilibria: an Alternative to Phyletic Gradualism. Models in Paleobiology. T. J. M. Schopf. San Francisco, Freeman Cooper: 82-115.

           

Gould, S. J. (1977). Ontogeny and Phylogeny. London, The Belknap Press of Harvard University Press.

           

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

           

Kipling, R. (1902). Just So Stories. London, MacMillan and Co.

           

Medawar, P. (2006). The Strange Case of the Spotted Mice and Other Classic Essays on Science. Oxford, Oxford University Press.

           

Williams, G. C. (1966). Adaptation and Natural Selection. Princeton, Princeton University Press.

           

Phenotype limited male mating tactics

I here attempt to extend the general overview of what looks like size determined mating tactics of male midges (McLachlan 2012). The available evidence now suggests that there may be, not one but three male phenotypes; ά, β and γ; thus the mating system of these flies may be more complex than previously imagined. Furthermore quite different mating behaviours appear to be associated with each male phenotype. The γ are the smallest and adopt a sit and wait behaviour under the mating swarm. These appear to intercept arriving females resting before entering the swarm. The mating tactic of β males depends, by contrast, on agility to capture mates on the wing in mating swarms. But, like singing crickets, these males have limited endurance (Mowles 2014). It is here that the recently discovered role of wing beat harmonics may be the proximate requirement for a successful mating event (Gibson, Warren et al. 2010; McLachlan 2012). Finally, ά males, I suggest, enjoy good endurance and there is some evidence that, to capture a mate, these mimic the flight behaviour of a major predator of mating swarms (post SSD revised 24/10/2014). The three phenotypes may demonstrate a phenotype limited ESS (Maynard Smith 1982), where size is the trait of the adult male that determines mating tactic, within a genetically determined mating strategy. The approximate relative sizes of ά and γ males are shown in Fig. 1; β males are intermediate.

  

Fig.1. Approximate relative size of ά (left) and γ males of the common chironomid midge Chironomus plumosus.

If there are distinct male phenotypes these ought to be detectable in the size frequency distribution of males from mating swarms and from individuals in the grass under a swarm. Results are shown in Fig.2.

Fig. 2. From (McLachlan and Neems 1989).

These samples were taken by net sweep through male mating swarms (a) and from the vegetation under the swarm (b), (McLachlan and Neems 1989). Recall that what is being tested is evidence for the presence of three male phenotypes. The evidence in Fig. 2 encourages a prediction of distinct male phenotypes, notably in the vegetation (a,d), but sometimes also in the swarm (b), which strongly suggest the presence of a distinct phenotype. In one case (a) three distinct size classes suggest the presence of all three phenotypes, ά, β and γ. More examples of discontinuous distributions among both midge swarm and mating pairs appear typical, e.g. Fig. 4b (McLachlan and Neems 1989): Fig. 1a (McLachlan 1986): Fig. 1a (McLachlan and Allen 1987), not shown here.  

There is more. Changes in the size frequency distribution of males in the swarm as the evening proceeds show the average size of males in the swarm to increase with time. This is what would be expected if β and γ males progressively tire and leave the swarm to rest. In the chaoborid midge Chaoborus flavicans (Fig. 3), the average size of males in two swarms increases progressively (left hand column, rs=0.29, P<0 .005="" 112="" 94="" column="" flies="" hand="" nbsp="" p="" right="" rs="0.2," span="">

Fig. 3. Size frequency distribution in the midge Chaoborus flavicans at progressive times (i) – (iii) about 15 minutes apart during swarming. Sized classes containing the mean are shaded, n = number of flies measured. Size classes are at intervals of 0.1mm starting at 4.0 mm. The two columns represent samples from duplicate swarms. After (McLachlan and Neems 1989).

Decisive evidence in support of a three phenotype hypothesis might be provided by wing shape measurements. Wing shape measurements, as used by Outomuro and co-workers for damsel flies (Outomuro, Rodriguez-Martinez et al. 2014), provide a ready-made method applicable to the midges. Wing shape measurements can readily be obtained from wings removed for the fly and measured at 10 magnifications in the usual way (McLachlan 1986). I predict that results will show statistically significant functional differences in wing shape among male phenotypes. For midges, broad wings (i.e. low aspect ration wings) are known to be are associated with sustained flight and narrow ones (high aspect ratio), with aerobatic flight (McLachlan 1986).

As a first step in thinking about an hypothesis of phenotype limited mating among midges I assume that the male phenotypes are genetically determined, labelled strategies by Thornhill and Alcock (Thornhill and Alcock 1983), p286. This is a different case from a condition dependent mating behaviour discussed by West-Eberhard (West-Eberhard 2003) and Thornhill and Alcock (Thornhill and Alcock 1983), p296-293 which concerns flexible phenotypic responses within a single genotype. Based on a premise of strategies together with findings and conjecture presented here, I suggest that three male phenotypes may form an evolutionarily stable strategy in the sense that it is uninvadable by mutants of the same size but with different mating behaviours. To be an ESS all three tactics would have to carry an equal fitness payoff. Any change in behaviour would be inconsistent with the size of the individual and thus carry lower fitness benefits leading to selection against the mutant. It has been suggested by my colleague John Lazarus, that we are not here dealing with a classical  ESS game but rather with the rock-paper-sissors evolutionaly game (Sinervo & Lively 1996).  This game relaxes the need for equal fitness payoff and has great explanatory power. 

Three distinct male phenotypes appear in quite a different classes of animal, namely the isopod crustacean Paracerceis sculpta (Shuster and Wade 2003), and in three species of Calopteryx damsel flies (Outomuro, Rodriguez-Martinez et al. 2014). For the isopod Paracerceis, Shuster and Wade provide a detailed analysis of phenotype limited mating tactics. The fact that three male phenotypes are found in this completely different class of animals hints that body size based strategies may turn out to be common, or even a near universal evolved solution to size based male intrasexual competition.

To recap; the hypothesis to be tested is that the mating system of the male chironomid and chaoborid midges involves at least three, phenotype limited mating strategies, based on body size and correlated differences in wing shape. To test this hypothesis good samples are required of males in mating swarms, in the vegetation under swarms and of mating pairs from both swarms and vegetation. For anyone who knows how to find mating swarms this should not be too difficult to achieve and could result in the untangling of the components of the baffling mating system of these ubiquitous insects. More work is needed to tie in functional difference in wing shape.

References

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.

           

Maynard Smith, J. (1982). Evolution and the Theory of Games. Cambridge, UK, Cambridge University Press.

           

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

           

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

           

McLachlan, A. J. (2012). SWARM BASED MATING SYSTEMS (revised May 2019). http://www.atholmclachlan.blogspot.com/.

           

McLachlan, A. J. and D. F. Allen (1987). "Male mating success in Diptera: advantages of small size ." Oikos 48: 11-14.

           

McLachlan, A. J. and K. J. MacLeod (In Preparation). "Sexual dimorphism in the chironomid midge - is it interesting?".

           

McLachlan, A. J. and R. M. Neems (1989). "An Alternative Mating System in Small Male Insects. ." Ecological Entomology 14: 85-91.

           

Mowles, S. L. (2014). "The physiological cost of courtship: field cricket song results in anaerobic metabolism." Animal Behaviour 89: 39-43.

           

Outomuro, D., S. Rodriguez-Martinez, et al. (2014). "Male wing shape differs between condition-dependent alternative reproductive tactics in territorial damselflies." Animal Behaviour 91: 1-7.

Sinervo, B., and Lively, C. K  (1996). The rock-paper-scissors game and the evolution of alternative male strategies. Nature, 380, 240-243, & 198-199.

           

Shuster, S. M. and M. J. Wade (2003). Mating Systems and Strategies. Princeton, Princeton University Press.

           

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.

           

Further discussion with John Lazarus has lead to the following note added on 23 July 2016:

Alternative male midge mating tactics and the Rock-Paper-Scissors Game

John Lazarus

Centre for Behaviour and Evolution, Newcastle University

In the original Rock-Paper-Scissors (RPS) children’s two person game each player simultaneously chooses one of three plays by showing their hand: a closed fist (Rock); an open palm (Paper) or two splayed fingers (Scissors). The rules are that Scissors cut Paper; Paper wraps Rock; and Rock blunts Scissors. Therefore each strategy beats one other and is beaten by the third, so there is no single winning strategy.

If the game is played in evolutionary time there will be a cycling in the frequency of strategy types over time since as one strategy increases in frequency this benefits the one that beats it but is worse for the one it beats. 

There is evidence for an evolved set of RPS strategies in a male lizard (Sinervo and Lively 1996). Might RPS also explain the three male midge strategies described here? We don’t know at present but here are some thoughts on the matter.

1. Although the 3 types don’t compete directly, as in RPS, the RPS evolutionary scenario would apply if the success of each type was frequency dependent in the following way. It would need to be the case that each type did better when there was an increase in the frequency of one of the other two types but worse when there was an increase in the other.

It seems that this might be the case. In the first place if there are fewer gammas intercepting females then males in the swarm would be expected, as a whole, to have higher mating success. However, it would need to be the case that one swarm type did better as gamma frequency declined but the other type did worse. This could happen in the following way. It is known that at any one time in the swarm betas have higher mating success than alphas due to their greater aerodynamic prowess (Crompton, Thomason, and McLachlan 2003;

McLachlan 2011). To simplify the argument assume that all females entering the swarm are taken by betas until all betas have left the swarm with a mate; above this threshold number of females alpha males start to get matings and increase their success as female entry rate increases further, while beta mating success remains constant (all betas having mated). Recall that female entry rate increases as gamma male frequency declines.

To summarise: for betas, below the threshold female number their success increases with female numbers, and above the threshold stays constant. For alphas it is the reverse; below the threshold their success is zero (in this simplest case) and above the threshold their success increases with female numbers. This picture fits the RPS scenario but with the complication of a threshold effect. And the threshold effect will be weakened in the real world, where some 
.alphas do get matings in the presence of betas.

2. If the 3 types are genetically distinct, as Athol Mclachlan suggests, then natural selection acting on an RPS system would result in cycling of the frequencies of the 3 types over generations. To test for such cycling one would need to be able to define a midge population in the field. 

3. The same logic might predict cycling fluctuations in male numbers in and around swarms over a single evening if males move between swarms to increase their mating success.

Athol comments on the RPS reasoning that John's ideas are testable. There are at least two testable hypotheses. First, do males move between swarms differentially depending on size? This can be tested using my swarm marking techniques. (McLachlan 1997). Second, do frequencies of the 3 phenotypes change in a swarm over time. This too is testable with the usual net sweep samples of swarms followed by wing length measurements (e.g. McLachlan and Allen 1987). 

References

Crompton, B., Thomason, J. and McLachlan, A.J. (2003). Mating in Viscous Universe: the Race is to the Agile, not to the Swift. Proc. R. Soc. London (B), 270: 1991-1995.

McLachlan, A. J. (1997). Size or symmetry: an experiment to determine which of the two accounts for mating success in male midges. Ecoscience, 4: 454-459.

McLachlan, A. J. (2011). Phenotypic Plasticity and Adaptation in a Holometabolous Insect: the case of the Chironomid midge. ISRN Zoology doi: 10.5402/2011/152342.

McLachlan, A. J. and Allen, D. F. (1987). Male mating success in Diptera: advantages of small size. Oikos 48: 11-14.

Sinervo, B., and Lively, C. M. (1996). The rock-paper-scissors game and the evolution of alternative male strategies. Nature, 380, 240-243 & 198-199 (the latter pages being a commentary by John Maynard Smith). 

Understanding Swarm-Based mating systems.

In September last year the Royal Entomological Society held a conference at St Andrews University entitle, Thirty Years of Thornhill and Alcock, The Evolution of Insect Mating Systems. The  conference has prompted to reread their book. The authors reveal, as never before, the adaptive complexity of the mating behaviour of the insects. In this light I examine again the taxon I know best, the chironomid midges, and attempt resolve the central question - is the mating system monogamous (males with only one partner)? 

We are slowly gaining ground in understanding the proximate aspects of the functioning of swarm-based mating systems, (see  ‘Swarm Based Mating Systems – the latest. 12/03/2012), but we are further behind  in understanding the ultimate, that is evolutionary, aspect of the functioning of these swarms. I have consistently assumed that the mating system of the chironomids is essentially monogamous. My reason for this is that, like mayflies, chironomids are short lived as adults and hence probably have only a single opportunity to mate. Under this assumption life time mating success and mating in a single evening are equivalent. By contrast with the vertebrates, this feature of the life cycle greatly simplifies studies of chironomids. An assumption of monogamy finds support in the fact that the heavily male biased operational sex ration, which is a feature of mating swarms, also favours an explanation of monogamy (Thornhill and Alcock 1983), p231. If not monogamy we are confronted by a mating system comparable in complexity to that of  the (Andersson 1994). And there is reason to be cautious about an assumption of monogamy. Confounding observations are of at least two kinds. First, the male external genitalia of chironomid midges are extraordinarily elaborate (Fig. 1.).  From (Armitage, Cranston et al. 1995)

Arnqvist (Arnqvist 1998), has shown that such complexity is the result of sexual selection on males in competition with rivals in polygyny (males have multiple partners) and/or polyandry (females have multiple partners). Second, unlike the mayflies, female chironomids possess spermathecae. This feature gives the female choice over what sperm to use in fertilising her eggs. It is difficult to imagine how the presence of spermathecae could have evolved if only one male fertilises her (Thornhill and Alcock 1983), p.325 et seq. Tests of these hypotheses are rare and when present often contradictory. For example, there is a contradiction between the findings of Downe (Downe 1973) and Arqvist (Arnqvist 1998), for the chironomid Chironomus riparius. But I  cautiously stand by an assumption of monogamy until further evidence is forthcoming.

For anyone with the inclination and expertise to do so, there are several tried and tested methods to explore the question of the mating system of the chironomid midge. For example, Downe (Downe 1973), uses radioisotopes to distinguish between the ejaculate of different males. Arnqnist (Arnqvist 1998) reviews the use of spermatophore counts in the female spermathecae. Some simpler observations could help. For example, the presence of various forms of plug left in the female genitalia after copulation could suggest monogamy (Thornhill and Alcock 1983), p240.  

References

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

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

                       

Arnqvist, G. (1998). "Comparative Evidence for the Evolution of Genitalia by Sexual Selection." Nature 393: 784-786.

Downe, A. E. R. (1973). "Some Factors Influencing Insemination in Laboratory Swarms of Chironomus riparius (Diptera: Chironomidae)." Canadian Entomologist 105: 291-298.

           

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

           

On the feet of elephants

Pools of rain-water in the axils of leaves, in tree hollows, on the surfaces of expanses of rock and in the foot-prints of large herbivores, are ubiquitous everywhere and may number in the millions of habitats for freshwater dwelling organisms; reviewed by  (McLachlan and Ladle 2001). They are inhabited by a great variety of aquatic animals, both invertebrate and vertebrate, sometimes indigenous and at great densities. Indeed, a case might be made that they are by far the principal fresh-water habitats on earth and hence also the source of much of the adaptive evolution among fresh water dwelling organisms. They are therefore a good place to identify adaptation. Because these small bodies of water are numerous and often occur in arid places, they provide an important focus for the activities of a variety of vertebrates, including birds, primates, viverrids, elephants and many others, all seeking drinking water. 

The activity around these puddles lead to an interaction with the pool inhabitants in unexpected ways. It is these interactions that provide the substance of my essay. Because pools typically dry after a short period, a central adaptation is dispersal. Charles Darwin (1859), regards pools as ‘island’ habitats and makes the point that their fauna may need help in achieving dispersal, this being provided by birds, among others, …”dispersal of their seeds by animals, more especially by fresh water birds, which have great powers of flight, and naturally travel from one piece of water to another”.

Interactions between the terrestrial and aquatic ecosystems often involve food. In tropical Africa viverrids (civets and genets), use the pools as lavatories, thus unintentionally providing a rich source of food for invertebrates in what may otherwise be a nutritionally poor habitat. The consequence is a flourishing population of biting midge larvae of the family Ceratopogonidae, not always welcome to humans. Such additions from the terrestrial environment can be too much of a good thing. My colleague Bram Vanschoenwinkel, reporting on the work of Brian Timms, tells me that the droppings of kangaroos, feral goats and human tourists, have lead to the pollution of rain-pools of Ayres Rock in Australia leading to dead pools and the possible total extinction of an indigenous fairy shrimp.

I now arrive at the point I really want to develop – the interactions between rain pool dwellers and elephants. As for as I am aware this relationship has never been formally investigated, but see (Vanschoenwinkel, Waterkeyn et al. 2011). Early in the 1960s it became apparent to me that something interesting followed from the routine bathing activities of elephants. My observations were made on the shores of Lake Kariba in the Zambezi valley.  In the rainy season the puddles of rain water in the foot prints of elephants on soft, wet ground after rain prove attractive to elephants. Their  foot prints are about 18 inches across and perhaps 6 inches deep. Scooping up water and mud to apply to their backs, perhaps to provide relief from heat, tsetse flies etc, deepens the foot print, eventually leading a pool several metres wide and perhaps half a metre deep. Such pools are inhabited by aquatic plants (Marsilia), and fairy shrimps (Chirocephalus), or in some cases ny the shrimp Lepidurus (Fig. 1). As far as I can tell, these organisms are found nowhere else in the Zambezi valley. Thus the activity of elephants leads to the creation of a unique fresh water habitat (Fig. 2, Fig. 3).

Here is an interesting opportunity for someone. I would start with the question of where Lepidurus and Chirocephalus come from. My prediction is that they will turn out to be carried as a resistant egg (Hildrew 1985), just like those on the feet of Darwin’s birds, but  by elephants moving from pools to pool with mud on their feet. Thus elephants may be solely responsible for the existence of this extraordinary habitat. Devising a sampling method to test such a hypothesis will require an inventive mind.

Fig. 1. The biota of elephant ponds. The floating leaves and submerged fruits of Marsilia (left) and the pond shrimps Lepidurus (top right) and Chirocephalus (below right).

Fig. 2. A rain pool created by the elephants shown in Fig. 3 below with Sandra McLachlan making observations in the rainy season 1964.

Fig. 3. The group of elephants observed in pool making activities. The pink colour is due to mud thrown on their backs.

References

Darwin, C. (1859). The Origin of Species by means of Natural Selection or the Preservation of Favoured Races in the Struggle for Life. Sixth edition, John Murray, London. Popular impression of the corrected copyright edition. 

         

Hildrew, A. G. (1985). "A quantitative study of the life history of a fairy shrimp (Branchiopoda: Anostraca) in relation to the temporary nature of its habitat, a Kenyan rain pool. ." Journal of Animal Ecology 54: 99-110.

           

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.

           

Vanschoenwinkel, B., A. Waterkeyn, et al. (2011). "Passive external transport of freshwater invertebrates by elephant and other mud-wallowing mammals in an African savannah habitat." Freshwater Biology 56: 1606-1619.

           

Niche Construction

When I first encountered the idea of Niche Construction some years ago, the impression I got was that the authors were ecologists who had strayed into evolution theory. They appeared to have re-invented concepts such as the Red Queen hypothesis (Van Valen 1973), phenotypic plasticity (West-Eberhard 2003), and the extended phenotype idea (Dawkins 1999), as well as long standing seral succession theory; e.g. (Clements 1916), and rolled them all together under one umbrella as a Darwinian process. There were also hints of mysticism touching on Gaia (Lovelock 1995). Re-reading some of the stuff last week (Jones 2005; Post and Palkovacs 2009), I was struck again by the same thoughts and yet, judging from comments on Google, the idea has garnered much support end even hyperbole, including two Nature papers, special conferences, a text book (Odling-Smee, Laland et al. 2003), and enthusiastic praise by prominent people such as Robert May and Richard Lewontin. Anything attracting so much attention is not easy to ignore.

I find that Richard Dawkins (Dawkins 2004), dismisses the Niche Construction idea on the grounds that it attempts to role together into one grand theory, Darwinian inheritance and non-Darwinian effects (echoes of Gaia again?). Among the latter are succession, accumulation of excretory products and oxygen generation all coming together, along with things like nest construction, under the heading ‘ecological inheritance’. The authors make some thought provoking points but from the evolutionary perspective it sounds like nonsense and I am inclined, like Dawkins, to dismiss the whole thing. Dipping into the Odling-Smee et al. text book, I have no reason to change my mind. Most telling, I can find nowhere that they address the point raised by Dawkins. We will have to wait and see if the idea survives the test of time. I am ready to be proved wrong.

References

Clements, F. E. (1916). Plant Succession. Washington, Carnegie Institute.

           

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

           

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

           

Jones, D. (2005). "Personal Effects." Nature 438: 14-16.

           

Lovelock, J. E. (1995). The Ages of Gaia. Oxford, Oxford University Press.

           

Odling-Smee, F. J., K. N. Laland, et al. (2003). Niche Construction. The Neglected Process in Evolution. Princeton, Princeton University Press.

           

Post, D. M. and E. P. Palkovacs (2009). "Eco-evolutionary Feedbacks in Community and Ecosystem Ecology: Interactions between the Ecological Theatre and the Evolutionary Play. ." Philosophical Transactions of the Royal Society (B). 384: 1629-1640.

           

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

           

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