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Selective Bird Predation on the Peppered Moth: the Last Experiment of Michael Majerus

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Selective Bird Predation on the Peppered Moth: the Last Experiment of Michael Majerus Selective Bird Predation on the Peppered Moth: The Last Experiment of Michael Majerus The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Cook, Laurence M., Bruce S. Grant, Ilik J. Saccheri, and Jim Mallet. 2012. Selective bird predation on the peppered moth: The last experiment of michael majerus. Biology Letters 8, no. 4: 609-612. Published Version doi:10.1098/rsbl.2011.1136 Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:11210622 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA Biol. Lett. (2012) 8, 609–612 took place in step with changing patterns of industrializ- doi:10.1098/rsbl.2011.1136 ation in Britain and elsewhere [3–5]. The melanic Published online 8 February 2012 ‘carbonaria’ morph is inherited via a dominant allele, Evolutionary biology C, at a single locus. The recessive c allele specifies the non-melanic black and white ‘typica’ form, while intermediate melanic ‘insularia’ alleles, inherited at the Selective bird predation on same locus, are dominant to typica and recessive to carbonaria. Insularia forms also increased, somewhat the peppered moth: the last variably, during industrialization [5]. Recently, this locus has been mapped and cloned; the pattern of gen- experiment of Michael etic variation in the genomic region harbouring the Majerus C locus suggests a rapid selective sweep around a single mutational origin of melanism [6]. L. M. Cook1, B. S. Grant2, I. J. Saccheri3 Melanics were long believed to be advantageous in and J. Mallet4,5,* the face of bird predation against bark resting sites dar- 1Life Sciences, University of Manchester, Manchester M13 9PT, UK kened by soot pollution [2], a form of camouflage [7]. 2Department of Biology, College of William and Mary, Williamsburg, Classic experiments in the mid-twentieth century VA 23187, USA proved that birds attacked the moths. Furthermore, rest- 3 Institute of Integrative Biology, University of Liverpool, ing moths that failed to match their background were Liverpool L69 7ZB, UK 4Genetics Evolution and Environment, UCL, 4 Stephenson Way, more vulnerable to bird predation in cage experiments London NW1 2HE, UK [8,9]. Mark–recapture studies of live moths, as well as 5Department of Organismic and Evolutionary Biology, Harvard many bird predation experiments using dead moths University, 26 Oxford Street, Cambridge, MA 02138, USA pinned to tree trunks, supported the hypothesis that *Author for correspondence ([email protected]). birds were the agents of selection on melanism [3,9]. Colour variation in the peppered moth Biston However, these procedures have drawbacks [3,5,10], betularia was long accepted to be under strong and critiques were increasingly aired [5,11,12]. In natural selection. Melanics were believed to be experiments, moths were often placed on tree trunks, fitter than pale morphs because of lower preda- which were argued to be abnormal resting sites; tion at daytime resting sites on dark, sooty bark. Melanics became common during the pinned carcases seemed particularly unnatural. Moths industrial revolution, but since 1970 there has were often released at greatly inflated densities, been a rapid reversal, assumed to have been potentially increasing predation. Reared insects from caused by predators selecting against melanics geographically distant sources were often used to sup- resting on today’s less sooty bark. Recently, plement wild individuals, and may not have behaved these classical explanations of melanism were as naturally in recapture experiments as wild moths. attacked, and there has been general scepticism By the 1990s, considerable scepticism became evident about birds as selective agents. Experiments [11–14]. Factors other than bird predation (e.g. and observations were accordingly carried out migration, physiological differences among genotypes) by Michael Majerus to address perceived weak- were argued to play a substantial role in the evolution nesses of earlier work. Unfortunately, he did not live to publish the results, which are analysed of melanism in Biston [5,15–17]. Caveats about the pre- and presented here by the authors. Majerus dation experiments discussed in Majerus’s book [5], released 4864 moths in his six-year experiment, critiques by other biologists, as well as points made par- the largest ever attempted for any similar study. ticularly forcefully in a review of the Majerus book [18], There was strong differential bird predation were soon exploited by non-scientists to promote an against melanic peppered moths. Daily selection anti-evolution agenda and to denigrate the predation against melanics (s 0.1) was sufficient in mag- explanation [10]. Kettlewell’s original mark–recapture nitude and direction to explain the recent rapid experiments were later argued to be fraudulent [19] decline of melanism in post-industrial Britain. (quite groundlessly: see [3,10,20]). Judith Hooper, These data provide the most direct evidence yet author of this claim, also suggested that bats rather to implicate camouflage and bird predation as than birds might be the agents of selection [19]. Soon, the overriding explanation for the rise and fall of melanism in moths. both the public in general and even evolutionary biol- ogists began to doubt the bird predation story Keywords: natural selection; cryptic coloration; (electronic supplementary material, S1 [18]). ecological genetics; insectivorous birds; melanism; Majerus therefore decided to make key new field lepidoptera observations, and he also designed and carried out a massive new predation experiment, the largest pre- dation experiment ever performed (4864 released 1. INTRODUCTION moths) to answer his own and other criticisms of Melanism in the peppered moth Biston betularia led to earlier work [5,10,21]. In addition, to address the the earliest measurements of natural selection on a Men- possible effect of bat predation, Majerus released live delian locus in the wild [1,2]. Rapid nineteenth century moths in night-time experiments in multiple locations: increases in melanics, followed by more recent declines he found no significant differences in predation of 419 melanic and typical moths eaten by three species of Electronic supplementary material is available at http://dx.doi.org/ pipistrelle bats [22]. 10.1098/rsbl.2011.1136 or via http://rsbl.royalsocietypublishing. org. Original source data from Majerus is given at http://dx.doi.org/ These results were all presented by Majerus in a 10.5061/dryad.962262h9 keynote address at the ESEB Congress, Uppsala, in Received 22 November 2011 Accepted 13 January 2012 609 This journal is q 2012 The Royal Society 610 L. M. Cook et al. Natural selection on melanism August 2007. Unfortunately, Majerus died after a Table 1. Numbers of wild peppered moths observed in short illness in 2009 before publishing the resting site different daytime resting positions, 2001–2006. Previous observations and predation results. However, the infor- authors had argued that moths rarely rested on tree trunks mation from the Uppsala talk, which forms the basis during the day, and that many predation experiments for the current analysis, was made freely available by employing tree trunks were therefore unnatural. In these new Majerus on the Internet soon thereafter as a set of pro- observations by Majerus, 35% of the 135 moths observed, both melanic and typical, were indeed found resting on jected slides. We have formed the current collaboration tree trunks. in order to analyse these results and disseminate them in print for the first time, as well as to clarify the impor- trunks branches twigs total tance of these key results for our understanding of natural selection in the wild. males 28 40 11 79 females 20 30 6 56 totals 48 70 17 135 2. MATERIAL AND METHODS Experimental and observational work presented here was carried out by Michael Majerus in a 1 ha rural garden, at Springfield, near His recent extensive observations on resting sites Coton, Cambridgeshire, UK. Full methods were published in a little-known chapter [10]; relevant extracts are provided here (elec- obtained while climbing the trees in his garden to set tronic supplementary material, S2). Original source files of his up the predation experiment appear to have been presentation in 2007, which contain the results analysed here, are lost, but he summarized the work in his 2007 provided at http://dx.doi.org/10.5061/dryad.962262h9. In cases Uppsala presentation (http: dx.doi.org/10.5061/ where numerical data were not supplied in these files, we have // expressed the results in terms similar to those used by Majerus in dryad.962262h9). An annotated version of this sum- the 2007 documents. mary is presented here. Majerus reported the following major features (table 1): (a) Natural resting sites While climbing trees in the experimental site in order to set up — The majority (52%) of moths rest on lateral sleeves for the predation experiment (see below), Majerus systemati- cally scrutinized trunks, branches and twigs of a limited set of trees branches. and recorded natural resting positions of all wild moths he found. — Of the moths on lateral branches, the majority The 135 observations he obtained here add considerably to the (89%) rest on the lower half of the branch. less-extensive resting site data previously published [10,12]. — A significant proportion of moths (35%) rest on (b) Predation experiment tree trunks. The purposes of the new experiment by Majerus were to estimate the — Of those that rest on trunks, the majority (87%) relative survival of local melanic and non-melanic moths at low, natur- rest on the north, rather than the south half. alistic densities. Moths (melanic carbonaria and non-melanic typica;no — A minority of moths (13%) rest under or among insularia morphs were used) were therefore released on substrates that Majerus himself had shown were normal for the species.
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