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Spite in Social Insects Areas CORRESPONDENCE 2 Schilthuizen, M. and Gittenberger, E. (1994) appears that the width of the hybrid zone is Bimodal hybrid zones and Parallel evolution of an sAat ‘hybrizyme’ in primarily affected, thus leading to difficulty in the scale of a snail hybrid zones in Albinaria hippolyti (Boettger). choosing a suitable sampling scale. However, Heredity 73, 244–248 the degree of bimodality can also vary. As 3 Schilthuizen, M. and Lombaerts, M. (1995) Life with sympatric sibling species4, the local In their recent TREE perspective, Jiggins and on the edge: a hybrid zone in Albinaria strength of disruptive natural selection Mallet discussed the intriguing distinction hippolyti from Crete. Biol. J. Linn. Soc. might vary in space and time. Alternatively, between unimodal hybrid zones (where the 54, 111–138 habitat and population structure, leading to hybrid zone is made up largely of recombinant 4 Schilthuizen, M. and Lombaerts, M. (1994) differences in dispersal pattern, can have genotypes) and bimodal zones (where Population structure and levels of gene flow in similar effects: in Bombina hybrid zones, most 1 recombinants form the minority) . They the Mediterranean land snail Albinaria populations are unimodal but some are nearly indicated that bimodality is associated with corrugata (Pulmonata: Clausiliidae). Evolution bimodal where the habitat is more patchy2. assortative mating, and that it might be the 48, 577–586 Although in individual cases it is often difficult stage where parapatric speciation and to determine whether divergence between reinforcement take place. hybridizing taxa occurred in situ or in Two aspects of uni- or bimodality remain allopatry, such variation in bimodality is unexplored in their paper. The first of these exactly the pattern expected if hybrid zone is the fact that deciding whether a zone is uni- Reply from C.D. Jiggins populations represent transitional stages in a or bimodal depends on the sampling scale. process of gradual parapatric speciation. A unimodal hybrid zone would be classified and J. Mallet as bimodal if the sampling area was larger Chris D. Jiggins than the zone itself, which is a real Schilthuizen’s comments1 highlight two James Mallet possibility in organisms where limited important aspects of bimodality in hybrid capacities for dispersal produce extremely The Galton Laboratory, University College zones. First, perhaps we did not emphasize London, 4 Stephenson Way, London, narrow hybrid zones. The second aspect, enough that, when identifying bimodality and UK NW1 2HE ([email protected]; which might warrant more attention, is the measuring linkage disequilibria within a zone, [email protected]) fact that a single hybrid zone might be it is critically important that samples represent unimodal in some places and bimodal in locally panmictic populations2. It is a well References other places, depending on the environmental known result of standard population genetics 1 Schilthuizen, M. (2000) Bimodal hybrid zones circumstances. that mixing geographic samples with and the scale of a snail. Trends Ecol. Evol. Both these phenomena are present in the divergent gene frequencies will create artificial 15, 469 hybrid zone between the land snails Albinaria heterozygote deficits and linkage disequilibria; hippolyti aphrodite and Albinaria hippolyti it is the local bimodality and concomitant 2 Jiggins, C.D. and Mallet, J. (2000) Bimodal harmonia in Crete. This zone runs for a deviations from Hardy–Weinberg or linkage hybrid zones and speciation. Trends Ecol. Evol. distance of approximately 10 km along a cliff equilibrium that are of special interest in the 15, 250–255 where rugged terrain changes into more study of speciation. Of course, in practice, 3 Feder, J. (1998) The apple maggot fly Rhagoletis gently undulating hills2. In places where the ‘local populations’ might be difficult to define. pomonella. Flies in the face of conventional environmental transition is gradual, the If present, bimodality should be evident at the wisdom about speciation? In Endless Forms: hybrid zone is more than 300 m wide. Where smallest spatial scale at which it is feasible to Species and Speciation (Howard, D.J. and the ecotone is more abrupt, the hybrid zone sample, provided this is small relative to the Berlocher, S.H., eds), pp. 130–144, can be as narrow as a few metres. Using a dispersal distance of the organism concerned. Oxford University Press standard sampling area of 10 3 10 metres We would probably consider the Albinaria 4 Grant, P. (1999) Ecology and Evolution of (and based on morphological hybrid indices zone to be unimodal throughout because Darwin’s Finches (2nd edn), Princeton and allozymes3), we would have to classify ‘unimodality would appear at extremely small University Press the 300 m hybrid zone as unimodal and the sampling areas’. narrow hybrid zone as bimodal. Choosing a Bimodality can also be difficult to detect larger sampling area would render both because many loci might be undifferentiated. situations bimodal, whereas unimodality If there are few loci examined, each with small would appear at extremely small sampling frequency differences between taxa, many Spite in social insects areas. heterozygotes and pairwise recombinant The histographical representation of genotypes might be present locally, thus In a past TREE News & Comment, Gadagkar1 any hybrid zone should not be used to leading to unimodal distribution on a hybrid- asked the question ‘can animals be spiteful?’; infer speciation without reference to the index plot. Adding more loci, especially if that is, do they ever harm another without a ratio between the sampling area and the more strongly differentiated, will give greater gain in personal reproduction. The cited dispersal distance of the organism under statistical power to detect bimodality. On a examples1, the killing of chicks in gulls and study. As it happens, in Albinaria, dispersal plot of hybrid index, the two peaks might egg cannibalism in sticklebacks, were later is only of the order of one metre per year4, slowly pull apart as more loci are added. Part shown to be better interpreted as plain thus assortative mating and reinforcement of the problem is the loss of resolution selfishness2. This led Keller et al.2 to conclude are unlikely where the hybrid zone is wide involved in representing a multidimensional that ‘spiteful animals are still to be because parental types are not within (multilocus) property – bimodality – on a two- discovered’. Here, we draw attention to recent cruising range of one another, whereas dimensional hybrid-index plot. Likelihood work on conflict in insect societies, which they might be in the narrower sections of analysis of multilocus genotypes3 is a more reveals several clear examples of spiteful the zone. appropriate statistical method and should actions. detect bimodality with greater sensitivity; The first class of examples are behaviours Menno Schilthuizen hybrid-index plots2 are merely a useful means that Wilson3 termed spiteful. He proposed that Institute for Tropical Biology and of data display. harmful behaviour could, in the absence of Conservation, Universiti Malaysia Sabah, Second, there is often considerable personal benefits, be favoured through Locked Bag 2073, 88999 Kota Kinabalu, variation between populations within a single benefits to a third party (Fig. 1). Consider sex- Malaysia ([email protected]) zone. Given the ubiquity of ecological ratio biasing in ants4, where workers kill their differentiation across hybrid zones, it is not brothers to increase the production of more References surprising that environmental variation, such valuable sister queens (fratricide; Fig. 1). 1 Jiggins, C.D. and Mallet, J. (2000) Bimodal as that described by Schilthuizen, should Fratricide, although detrimental to the male hybrid zones and speciation. Trends Ecol. Evol. affect the genetic structure of hybrid zone recipients, is not carried out to benefit the 15, 250–255 populations. In the case of Albinaria, it personal reproduction of the worker because TREE vol. 15, no. 11 November 2000 0169-5347/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved. 469 CORRESPONDENCE separates two distinct processes. Sex-ratio 7 Hamilton, W.D. (1970) Selfish and spiteful biasing could also occur through preferential behaviour in an evolutionary model. Nature feeding of sister larvae4 – nepotistic altruism, 228, 1218–1220 whereas it actually involves harm to males4 – 8 Hamilton, W.D. (1971) Selection of selfish and spite. Worker policing in honey bees5, where altruistic behaviour in some extreme models. workers invest time in the destruction of In Man and Beast: Comparative Social Behavior worker-laid male eggs, thus facilitating their (Eisenberg, J.F. and Dillon, W.S., eds), replacement with more valuable queen-laid pp. 57–91, Smithsonian Press male eggs5,6, is similarly spiteful (Fig. 1). 9 Keller, L. and Ross, K.G. (1998) Selfish genes: But, does Hamilton’s more stringent view of a green beard in the red fire ant. Nature spite ever occur7,8? He argued that spite could 394, 573–575 evolve with only two parties, but required 10 Hurst, G.D.D. and McVean, G.A.T. (1998) Selfish highly specific conditions7,8. Amazingly, the genes in a social insect. Trends Ecol. Evol. recently discovered ‘green-beard’ matricide in 13, 434–435 11 Grafen, A. (1985) A geometric view of the fire ant (Solenopsis invicta)9,10 has all the relatedness. Oxford Surv. Evol. Biol. 2, 28–89 conditions Hamilton predicted (Fig. 1): (1) kin Competition discrimination – a ‘green beard’ gene that (a) Fratricide enables workers to identify nongene carrier Worker Brother Sister queens; (2) a low cost to the actor – in fact, no cost because fire ant workers are sterile; and rR = 0.25 (3) negative relatedness, from the perspective Mitochondrial rX = 0.75 of the green beard locus, because the killed recombination or (b) Policing queens are less likely than random to possess the green beard gene10. As the antithesis of coevolution of sites? Worker Nephew Brother altruistic behaviour, the harm to non-kin is 1 sufficient to cause the spread of spite, without A recent TREE News & Comment by Hey , rR = 0.15 7,8 rX = 0.25 requiring any indirect benefits (Fig.
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