How Did the HornedLizard Get Its Horns?

IN THEIR BREVIA “HOW THE HORNED LIZARDgot its horns,” K. V. Young et al. present animportant example of natural selection in thewild, suggesting that loggerhead shrike preda-tion drove the evolution of elongated horns inthe flat-tailed horned lizard (2 Apr., p. 65).Although the authors acknowledge that selec-tive forces other than shrike predation mayalso be involved, they make no mention of thepossibility that one of these potential forcescould have been the first instigator of thedirectional selection for horn elongation.Under this hypothetical scenario, the hornswould have then only subsequently served toreduce shrike predation. Other likely cases ofpreadaptation [or exaptation (1)] have beendescribed in vertebrates (2–5), some of whichinvolve important transitions in evolutionaryhistory. Perhaps the role of preadaptation inevolution is of great importance and is de-serving of more widespread appreciation.Given the possibility of a preadaptationscenario in the evolution of crown horns inhorned lizards, I find it ironic that Young et al.commented on the weakness of “just-sostories” (6) and also chose a title that readsremarkably like the titles of Kipling’s stories.Until presented with evidence suggesting thatthe horns were mere nubs until the onset ofshrike predation, I will remain convinced that“How the horned lizard got its horns” is apoor choice for what is presumably meant tobe an informative title.

WILLIAM R. FOUTS

Department of Biology, Nevada State College, 1125Nevada State Drive, Henderson, NV 89015, USA.

References1. S. J. Gould, S. Vrba, Paleobiology 8, 4 (1982).2. K. P. Dial, Science 299, 402 (2003).3. S. J. Gould, The Panda’s Thumb (Norton, New York, 1980).4. D. J. Futuyma, Evolutionary Biology (Sinauer,

Sunderland, MA, ed. 3, 1998).5. N. H. Shubin et al., Science 304, 90 (2004).6. R. Kipling, Just So Stories (Doubleday, New York, 1902).

IN THEIR BREVIA “HOW THE HORNED LIZARDgot its horns” (2 Apr., p. 65), K. V. Young etal. claim to have direct evidence of thedefensive function of the long bony horns

that fringe the lateral and posterior marginsof the head of the flat-tailed horned lizard(Phrynosoma mcalli). They show elegantlyand convincingly that loggerhead shrikes(Lanius ludovicianus) prey on lizards withrelatively short horns (corrected for bodysize) and that this source of mortalityproduces directional selection favoringlonger horns. Unfortunately, the authorsincorrectly conclude that “defense againstshrike predation is one factor driving theradical elongation of horns in some speciesof horned lizards.” This conclusion isincorrect because they did not show thatthe lizards use their horns to defend them-selves against shrikes, nor did they showthat longer horns are better for defense.Suppose that lizards with longer horns alsoare more vigilant, escape faster, spend lesstime in the open, are more cryptic, or haveother traits that reduce the chance they areseen, caught, killed, and eaten by shrikes.Any of these correlated traits could alsoexplain the observed pattern of predationand selection. Observations of how shrikesattack lizards and how lizards defendthemselves, and measurements of preda-tion rates on lizards with experimentallyshortened and lengthened horns are neededto test the validity of the intuitively attrac-tive suggestion that the horns of hornedlizards are defensive. At present, thisexplanation for the adaptive function forhorns remains a “just-so story.”

JOHN H. CHRISTY

Smithsonian Tropical Research Institute, Apartado2072, Balboa, Ancon, Panama. E-mail: chirstyj@naos.si.edu

IN THEIR BREVIA “HOW THE HORNED LIZARDgot its horns” (2 Apr., p. 65), K. V. Young etal. explain the causal processes of how theflat-tailed horned lizards (Phrynosomamcalli) developed parietal horns as adefense against the impaling capabilities ofthe loggerhead shrike (Lanius ludovi-cianus). However, the actual selectionfactor that the horns help to defend thelizards from—how shrikes kill their verte-brate prey—was not discussed. Shrikesprey differentially on invertebrates andvertebrates. A shrike (Lanuis spp.) kills itsvertebrate prey (1, 2), including speciesthat may weigh as much as an adult shrike(30 to 75 g depending on the species ofshrike), with a bite directed at the portionof the prey’s neck immediately posterior tothe skull. The bite disarticulates the verte-bral column. When the prey is dead, ashrike will fly to a convenient perch where

the prey is either impaled on a sharp pointor dragged and lodged into a fork of abranch (3). This allows a shrike to pull theprey apart with its bill into portions thatcan be swallowed.

Natural selection can only occur if indi-viduals survive a given experience and areable to transmit that information to con-specifics or their progeny (4). Given mylong experience in the field with shrikes,the attack period is the only possible eventwhen a horned lizard could experience andescape the attacks of the shrike to the nape.Further, it is also possible that attacks byinexperienced juvenile shrikes, allowingfor a greater percentage of escapes (3), onthe horned lizards gave rise to the selectionfor elongated horns. It also does not makeevolutionary sense for a trait to be incorpo-rated into a prey species, as a result of apredator’s behavior, that results in all casesin its death (i.e., the impaling stage).Hence, although I accept the authors’conclusion that “defense against shrikepredation is one factor driving the radicalelongation of horns,” I suggest that theparietal horns developed as a defenseagainst shrike attacks to the nape regionand not against their being impaled afterthey are dead. Thus, the posterior-directed(and perhaps even the lateral-directed)cranial horns of a Phrynosoma lizard are apotential danger to a shrike, aimed as theyare at a shrike’s eye when it goes in for alethal bite at the lizard’s neck.

REUVEN YOSEF

International Bird Research Centre in Eilat,Department of Life Sciences, Ben-GurionUniversity of the Negev, Eilat 88000, Israel.

References1. T. J. Cade, E. C. Atkinson, Birds N. Am. 671 (2002).2. R. Yosef, Birds N. Am. 231 (1996).3. R. Yosef, Vogelwarte 42, 25 (2003).4. M. W. Strickberger, Evolution (Jones & Bartlett,

Boston, 1990).

Flat-tailed horned lizard in defensiveposture.

Letters to the EditorLetters (~300 words) discuss material publishedin Science in the previous 6 months or issuesof general interest. They can be submittedthrough the Web (www.submit2science.org)or by regular mail (1200 New York Ave., NW,Washington, DC 20005, USA). Letters are notacknowledged upon receipt, nor are authorsgenerally consulted before publication.Whether published in full or in part, letters aresubject to editing for clarity and space.

LETTERS

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Proteomics 4:

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24 SEPTEMBER 2004 VOL 305 SCIENCE www.sciencemag.org

Response THE TITLE OF OUR PAPER WAS MEANT AS ANallusion to the Just So Stories of Kipling(1), which are often used as a shorthandcriticism for unsubstantiated adaptive argu-ments. It is a bold statement, and wethought it so clearly over the top that itwould not be taken as a literal explanatorytitle. The problem of identifying adapta-tions and their causes has (at least) twoschools of thought, one that focuses on thesource of the original character statechange (as described by Fouts), and onethat focuses on current value and selection(as described in our Brevia). Heritabletraits that have current adaptive value, as isthe case for the horns of flat-tailed hornedlizards (Phrynosoma mcalli), will continueto change through natural selection,thereby leading to continued adaptationand explaining in part how horned lizardsgot elongated horns. The question ofwhether any horns on the head of hornedlizards existed before shrike predationdrove them to elongated states (i.e., were“preadapted”) is an interesting one, but onethat is only answerable through compara-tive analyses with full phylogenetic infor-mation and ancestral environmental condi-tions (2). Although we have not performedsuch an analysis and could probably neverreconstruct the ancestral predation condi-tions, it is worth noting that of the 13species of horned lizards currently extant,P. mcalli has the longest relative hornlengths and belong to the most derivedspecies group (3, 4), while some otherspecies in the genus (e.g., P. douglassi)have virtually no parietal or squamosalhorns (i.e., the nubs mentioned by Fouts).

Christy correctly points out the twoprimary shortcomings of any covarianceanalysis of selection: It is impossible to ruleout every unknown unmeasured character thatcould drive the observed selection, and covari-ance analyses usually cannot assign a mecha-nism of selection because they are not manip-ulative studies (5). In the case of shrike preda-tion selecting on horn length in lizards,however, we have measured a fitness compo-nent undeniably assignable to predation by asingle predator. We also know that lizardsroutinely use their horns behaviorally indefense, jabbing them backward into anythingthat restrains them, often with enough force todraw blood from human fingers. It seemsmost parsimonious to conclude that the fitnessadvantages conferred by longer horns withrespect to shrike predation accrue because oftheir defensive function, rather than to invokesome unknown correlated character thatgenerates the observed covariance.

Yosef describes the predation behaviorof shrikes attacking their prey and in doingso explains some of the critical natural

history driving the natural selection weobserved. We regret that space limitationsprevented us from fully describing thefascinating behavior of shrikes, and thecomments of Yosef help to fill in some ofthese blanks and support the interpretationsin our paper. The impaling behavior ofshrikes provides a unique sampling ofsuccessful predation, but we never intendedto imply that horn length served to preventthe impaling process per se.

The defensive behavior of flat-tailedhorned lizards is consistent with the inter-pretation that longer horns deter attacks byshrikes. When attacked or grasped, flat-tailed horned lizards stab their spines intothe offending object. In the case of humanfingers, this behavior often results inbleeding and immediate release of thelizard. The predation behavior of shrikes,which typically attack near the neck, wouldplace vulnerable areas of the predator’sface within range of the parietal andsquamosal horns of flat-tailed hornedlizards. Lizards with relatively longer hornswould be expected to be more likely to beable to reach and inflict damage on a pred-ator, thereby interrupting the predationsequence and escaping.

EDMUND D. BRODIE III,1 KEVINV.YOUNG,2

EDMUND D. BRODIE JR.21Department of Biology, Indiana University,Bloomington, IN 47405–3700, USA. 2Departmentof Biology, Utah State University, Logan, UT84322–5305, USA.

References1. R. Kipling, Just So Stories (Doubleday, New York, 1902),

p. 249.2. H. W. Greene, Fieldiana Zool. 31, 1 (1986).3. K. Zamudio, W. L. Hodges, Mol. Phylogenet. Evol. 31,

961 (2004).4. R. R. Montanucci, Contrib. Sci. Nat. Hist. Mus. Los

Angeles County 390, 1 (1987).5. E. D. Brodie III,A. J. Moore, F. J. Janzen, Trends Ecol. Evol.10, 313 (1995).

The Importance ofEducating Girls

INHIS EDITORIAL“SUSTAINABLE DEVELOPMENT”(30 Apr., p. 649), J. Sachs eloquently describesscientists’ increasing concern about the diffi-culty of providing for a growing global popu-lation in sustainable ways.

It will be much easier to achieve decent,sustainable living standards if populationgrowth slows more rapidly. Extensiveresearch from diverse countries shows thatwhile family planning and basic health careclearly play major (and reinforcing) roles,expanding education for women wherefemale education levels are now relativelylow is probably the single most effectiveway to encourage a shift to smaller,healthier, and better educated families (1,

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2). Education boosts women’s earningcapacity roughly as it does men’s (3–5).Education also improves women’s“bargaining position” in the family andsociety. As education and resulting higherearning capacity increase the opportunitycost of women’s time, couples tend to havefewer children and to invest more in thehealth and education of each child. AWorld Bank study of 100 countries findsthat when women gain four years of educa-tion, on average, fertility per woman dropsby about one birth (6), and another studyof 65 countries finds that doubling theproportion of women with a secondaryeducation from 19 to 38% would reduceaverage fertility rates from 5.3 to 3.9 chil-dren (and improve child mortality too) (2).

Yet despite the benefits of female educa-tion, the UN estimates that 104 millionschool-age children—60 million of themgirls—are not in school each year (7). TheWorld Bank reports that in sub-SaharanAfrica, more than half of girls do notcomplete a primary education (8). Onereason is that even basic education carriesconsiderable costs to parents—tuition maycome to one-fourth of poor families’incomes. (Even when education is suppos-edly free, “extra fees” and indirect costs forschooling may burden poor families.) Yet thebenefits of education accrue mainly to thegirls when they grow up, to the families theyhave in their turn, and to their societies, notimmediately to the parents who decide onschooling. The benefits may well seemdistant and dicey to the parents, particularlyin cultures where girls “marry out” andwhere poverty is widespread and the qualityof available education is very poor.

Many countries—from Bangladesh, toChina, to Mexico—have strong programsto improve education for girls and boys.But far more needs to happen to bringmore girls into school, ensure that theystay beyond primary school, and providethem decent quality education. Althoughmany if not most people support suchefforts, it’s a question of priority.

As Lawrence Summers emphasizedwhen at the World Bank and the TreasuryDepartment, once all its benefits areconsidered, female education may well bethe highest return investment available tothe developing world (9). The impact offemale education on family size and well-being—and so also on population growthand the prospects for sustainable develop-ment—is enormous. Female educationthus deserves far more priority in publicpolicy both in particular countries andinternationally. An international effortunder UN aegis is under way to achieve“Basic Education for All” by year 2015.Whether this effort accomplishes its goal

depends on greater national and interna-tional political commitment, on increasedfinancial support, on real educationreforms, and thus on greater public under-standing.

BARBARA HERZMoose, WY, USA.

References1. B. Herz, G. B. Sperling, What Works in Girls’ Education:

Evidence and Policies from the Developing World(Council on Foreign Relations, New York, 2004).

2. K. Subbarao, L. Raney, Econ. Dev. Cultural Change 44(no. 1), 105 (1995).

3. G. Psacharopoulos, H. A. Patrinos, “Returns toInvestment in Education: A Further Update,” WorldBank Policy Research Working Paper 2881 (WorldBank, Washington, DC, 2002).

4. T. P. Schultz, World Dev. 30 (no. 2), 207 (2002).5. T. P. Schultz, in Women’s Education in Developing

Countries: Barriers, Benefits, and Policy, E. King, M. A. Hill,Eds. (Johns Hopkins Univ. Press, Baltimore, MD, 1993).

6. S. Klasen, “Does Gender Inequality Reduce Growthand Development? Evidence from Cross-CountryRegressions,” Policy Research Report on Gender andDevelopment Working Paper No. 7 (World Bank,Washington, DC, 1999).

7. UNESCO, Education for All Global Monitoring Report2003/4 (UNESCO, Paris, 2003).

8. B. Bruns, A. Mingat, R. Rakotomalala. “AchievingUniversal Primary Education by 2015: A Chance forEvery Child” (World Bank, Washington, DC, 2003).

9. L. H. Summers, “Investing in All the People: EducatingWomen in Developing Countries,” EDI Seminar paperNo. 45 (World Bank, Washington, DC, 1994).

Future Global WarmingScenarios, Take 2

IN HIS LETTER “FUTURE GLOBAL WARMINGscenarios” (16 Apr., p. 388), W. S. Broeckercritiques our recent study for the Departmentof Defense on the national security implica-tions of abrupt climate change (1). Weadmire Broecker and his work, whichimportantly informed the scientific under-pinning of the study, and although we agreewith the substance of his comments on thescience of climate change, his critique doesnot accurately reflect the content of thereport—or its intent.

First, we make no predictions. As ouropening paragraph explicitly states: “Thepurpose of this report is to imagine theunthinkable—to push the boundaries ofcurrent research on climate change so wemay better understand the potential impli-cations on United States national secu-rity… We have created a climate changescenario that although not the most likely,is plausible, and would challenge UnitedStates national security in ways that shouldbe considered immediately.”

Broecker is correct in asserting that themost likely scenario is one of regionalclimate change (locations uncertain) manydecades from now. But that would havelittle impact on today’s strategic planningfor national security. That is why we exam-ined the plausibility of a low-likelihood,

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near-term abrupt climate change scenarioacross all the major geographies.

Why should abrupt climate changematter to the Department of Defense?Because thinking the unthinkable is funda-mental. In 2000, the senior writer of thisreport led one of the teams that explored“National Security in the 21st Century”with the Hart-Rudman Commission. TheCommission’s report, published in thesummer of 2001, concluded that a majorterrorist attack on U.S. soil was likely in thenext quarter century and that we were illprepared to either detect or stop it. At thetime, this was considered a low-probabilityevent; today, the government is underconsiderable fire for not seriously consid-ering such scenarios.

Our climate change study wasconducted and shared in that spirit. It wasnot an attempt to do climate science orinfluence climate policy. But its conclu-sions strongly suggest that it is in ournational security interests to increasesupport for climate science so that we cangain better insight into the timing, nature,and likelihood of abrupt climate change.

PETER SCHWARTZ AND DOUG RANDALL

Global Business Network, 5900 X Hollis Street,Emeryville, CA 94608, USA.

Reference1. P. Schwartz, D. Randall, “Abrupt climate change,” report

prepared by Global Business Network (GBN) for theDepartment of Defense, available at www.gbn.org/ArticleDisplayServlet.srv?aid=26231.

CORRECTIONS AND CLARIFICATIONS

Perspectives: Draft versions of the PDFs for threePerspectives (Busse, Stolow, and Levin) in the issue of10 Sept. were inadvertently posted. The correctversions were posted on 13 Sept. at approximately 4p.m. The HTML and print versions of these articleswere correct. If you downloaded a PDF of one of thesePerspectives prior to the above date, please return toScience Online to obtain the correct version.

Random Samples: “Reason to exist” (13 Aug., p. 941).Susan Ganter, the new executive director of theAssociation for Women in Science (AWIS), is on leavefrom her position as associate professor of mathe-matical sciences at Clemson University and remainsinvolved in educational and research activities. Theitem wrongly implied that she no longer has an affili-ation with Clemson and that she would not be contin-uing her work in mathematics and education.

Special Issue on Immunotherapy: Viewpoint:“Therapeutic vaccines for chronic infections” by B.Autran et al. (9 July, p. 205). The purple lines in panels(B) and (C) of Fig. 1 were printed incorrectly. Thecorrect figure appears here.Also, the authors would liketo acknowledge support from the European Union.

Reports: “Antigen bias in T cell cross-priming” by M. C.Wolkers et al. (28 May, p. 1314). Two of the symbols inFig. 3B were denoted incorrectly. The closed trianglesrepresent RMA-S sE7-GFP-NP cells, and the closedcircles represent RMA-S sNP-GFP-E7 cells.

Preventativevaccine No

infection

Pathogen

Expansion ofExpaExpaT/B effector cellsT/BT/BT/BT/B

Generation ofT/B memory cells

Re-expansion ofT/B effector cells

cTherapeuT euticcvaccines +

lsslssantimicroobialialantimicrobbb

Chronic infection Disease

Expansion ofT/B effector cells

Persistence ofspecific T/B cells

Exhaustion ofspecific T/B cells

Expansion oofT/B effector cecells

oofoPersistence ooecific T/B cellscellscellsspecific T/B ceecific T/B ce

expansion ofRe-e effector cellsT/B

Chronic infection No disease

A

B

C

TECHNICAL COMMENT ABSTRACTS

COMMENT ON “Role of NMDA Receptor Subtypes in Governing the Directionof Hippocampal Synaptic Plasticity”Dmitri A. Rusakov, Annalisa Scimemi, Matthew C. Walker, Dimitri M. Kullmann

Liu et al. (Reports, 14 May 2004, p. 1021) reported that NMDA receptors containing NR2A and NR2B subunits areselectively coupled to long-term potentiation (LTP) and long-term depression (LTD), respectively. Because NR2B (butnot NR2A) receptors occur outside synapses, and can be activated by glutamate spillover, this principle may underliesynaptic homeostasis.Full text at www.sciencemag.org/cgi/content/full/305/5692/1912b

RESPONSE TO COMMENT ON “Role of NMDA Receptor Subtypes in Governingthe Direction of Hippocampal Synaptic Plasticity”Tak Pan Wong, Lidong Liu, Morgan Sheng, Yu Tian Wang

Although we agree with Rusakov et al. that activation of extra-synaptic NR2B receptors by glutamate spillover maylead to heterosynaptic LTD,our data also support a role of synaptic NR2B receptors in homosynaptic LTD.The proposedrole of extrasynaptic NMDA receptor-mediated LTD in synaptic homeostasis may thus be temporally limited.Full text at www.sciencemag.org/cgi/content/full/305/5692/1912c

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