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selection. The principles of phenotypicvariation, corresponding variation infitness, and heritability are so simpleand seemingly inevitable in theirconsequences that the main questionis not “What are they?” or “Are theytrue?” but “Why should they beregarded as such a big deal?” To answerthis question, I ask the students toimagine how someone would explainthe properties of an organism beforeDarwin’s theory of evolution. Only twooptions would be available; theological(God’s handiwork) or material(explaining the properties of the wholefrom the properties of the componentparts). The big deal about naturalselection is that it provides a thirdexplanatory framework, different fromboth theology (this is already obviousto the students) and materialism (thisis not). To the extent that the materialcomposition of organisms results inheritable variation, it becomes a kindof living clay that can be molded byenvironmental forces that influencesurvival and reproduction. Themost interesting properties of a claysculpture are caused by the moldingaction of the artist, not the physicalproperties of clay. In the same way,evolutionary biologists routinely makepredictions about the propertiesof organisms (such as “many preyorganisms match their background toavoid detection by predators”) withoutany reference to the physical materialsof the organisms, including their genes.This is the fundamental distinctionbetween proximate and ultimatecausation in evolutionary biology,and it is the second major idea in thesequence that I attempt to convey tostudents. The distinction is importantbecause it has such predictive value.Knowing only a little about anorganism and its environment, one canmake predictions about its propertiesthat are not certain to be correct,but which are likely to be correct. Inmundane terms, they are good guesses.I make this point with a class exerciseof the sort recommended by Altersand Nelson. Choosing the subject ofinfanticide, I say that superficially itmight seem that organisms would neverevolve to kill their own offspring, butwith a little thought the students mightbe able to identify situations in whichinfanticide is biologically adaptive forthe parents. I ask them to form smallgroups by turning to their neighborsPLoS Biology www.plosbiology.orgto discuss the subject for five minutesand to list their predictions on a pieceof paper.After the lists are collected, Iask the students for some of theirpredictions to list in front of thewhole class. They are eager to talk,and reliably identify the three majoradaptive contexts of infanticide: lackof resources, poor offspring quality,and uncertain paternity, along with lesslikely possibilities, such as populationregulation, that can be set asidefor future discussion. I conclude byattempting to convey the simple butprofound message of the exercise:How can they, mere undergraduatestudents, who know almost nothingabout evolution and (one hopes) knownothing at all about infanticide, soeasily deduce the major hypothesesthat are in fact employed in the studyof infanticide for organisms as diverseas plants, insects, and mammals? Thatis just one example of the power ofthinking on the basis of adaptation andnatural selection.One explanatory framework, manyapplications. The next major ideato convey is that the same reasoningcan be applied to an infinite numberof topics. Why are males larger thanfemales in some species and the reversein others? Why are there two sexesin the first place? Why are males andfemales born in equal proportionsin some species but not others? Whydo some organisms reproduce onceand then die, while others reproduceat repeated intervals? Why do someplants live for three weeks andothers for 3,000 years? Why are someorganisms social and others solitary?Among social organisms, why do someindividuals cooperate and othersexploit? Predictions based on naturalselection provide a starting point forinquiry on all of these subjects, just aswith infanticide. Evolutionary theoryprovides an escape from the extremespecialization that characterizesso much of the rest of science. Ittranscends taxonomic boundariesbecause organisms as different asplants, insects, and mammals can besimilar in terms of their adaptations tosimilar environmental problems, forinfanticide and many other subjects. Ittranscends subject boundaries becausethe problem of how to select food (forexample) is very similar to the problemof how to select a mate. Evolutionary1003biologists sometimes take it forgranted that they possess a commonlanguage that can be spoken acrossso many domains of knowledge. It isan extraordinary fact and needs to bepresented as such to students learningabout evolution for the first time.Humans in addition to the restof life. One of the biggest tacticalerrors in teaching evolution is toavoid discussing humans or to restrictdiscussion to remote topics such ashuman origins. The question of howwe arose from the apes is fascinatingand important, but is only one of anynumber of questions that can be askedabout humans from an evolutionaryperspective—including infanticide. Ifevolutionary theory can make sense ofthis subject for organisms as diverseas plants, insects, and mammals, whatabout us? If we operate by differentrules than all other creatures for thisand other subjects, why should this beso? The most common answer to thisquestion is “learning and culture,” butwhat exactly are these things? Do theyexist apart from evolution, or do theythemselves need to be explained froman evolutionary perspective? I raisethese issues early in the course, not toanswer them, but to emphasize howmuch is “on the table” as part of thecourse.For millennia, humans haveregarded themselves as categoricallydifferent from other creatures intheir mental, moral, and aestheticabilities. We are obviously uniquein some respects, but in exactlywhat way needs to be completelyrethought. Nonhuman species havebeen discovered to be vastly moresophisticated and behaviorally flexiblethan most people imagined even 30years ago. They solve the recurrentproblems of their environments as wellas, or better than, humans. They canchange not only their behaviors buttheir entire bodies and life historiesin response to environmental change.Something happened several millionyears ago to give our species a specialkind of behavioral flexibility, and theability to socially transmit behaviorsin a cumulative fashion (culture). Asophisticated knowledge of evolutionis required to discover exactly whathappened. As for the consequencesof these new mental capacities, theydo not necessarily cause our speciesto play by a different set of rules thanDecember 2005 Volume 3 Issue 12 e364

other species. Perhaps they enable usto play the evolutionary game betterand faster than other species. For aspecific topic such as infanticide, it allboils down to an empirical question:Do people commit infanticide underthe same environmental conditions asother species? It turns out that there isa sizeable literature for this subject, tobe reviewed later in the course alongwith a more general discussion of thenature of human learning and culture.Students who become exceptionallyinterested are directed to a growinggenre of accessible and authoritativebooks, such as Jared Diamond’s Guns,Germs, and Steel [16–22].It might seem that boldly discussingsubjects such as human infanticide(which the students quickly connect tothe contemporary issue of abortion),along with other topics such as sexdifferences and homosexuality laterin the course, is the ultimate inpolitical incorrectness. However, Ihave taught this material for manyyears in prior courses without a singlecomplaint, and the assessment of“Evolution for Everyone” demonstratesan overwhelmingly positive responseacross the religious and politicalspectrum. Clearly, there is a way toproceed that arouses intense interestwithout animosity or moral outrage.In the case of infanticide, evolutionarytheory doesn’t say that it’s right—it isused to make an informed guess aboutwhen it occurs. All of the studentswant to know if the guess proves tobe correct for humans in addition toother creatures, regardless of theirmoral stance on abortion. Moreover,they see that the information can beuseful for addressing the problem,whatever particular solution they havein mind. The importance of culture isnot denied, but becomes part of theevolutionary framework rather thana vaguely articulated alternative. Thepicture that emerges makes senseof cases of infanticide that appearperiodically in the news (typicallyyoung women with few resourcesand under the influence of a malepartner who is not the father) andthat previously seemed inexplicable.Nearly everyone values this kind ofunderstanding and thinks that it canbe put to positive use, as demonstratedby the quantitative assessment. Moregenerally, including humans along withthe rest of life vastly increases students’PLoS Biology www.plosbiology.orginterest in evolution and acceptanceto the degree that it seems to lead tounderstanding and improvement of thehuman condition.Not everything is adaptive. Readersof this essay familiar with evolutionarytheory might be wondering why mysequence of ideas relies so heavily uponadaptation and natural selection up tothis point. Isn’t there more to evolutionthan natural selection, as Stephen JayGould cautioned at every opportunity[23–25]? The answer is “yes,” butthis point needs to come later in thesequence, after the basic concept ofadaptation and its explanatory powerhave been established. There aremany reasons why organisms are notperfectly adapted to their environment.There might be insufficient time,especially when the environmentchanges, as it does with a vengeancein our own species. The living clayof heritable variation is by no meansinfinitely malleable. There are hiddenconnections among traits based ongenetics and development, such thatselection for one trait drags othersalong. Gene frequencies change bydrift and mutation in addition toselection. The list goes on and on,and mature research programs inevolutionary biology pay attention to allof these factors.If so, then why should adaptationand natural selection enjoy a specialstatus? The answer is quite practical:It is usually much easier to make aprediction based on knowledge of theorganism in relation to its environmentthan predictions based on the otherfactors. In the case of infanticide,my students easily derived the majoradaptationist predictions, but would beat loss to derive predictions based onphylogeny, developmental and geneticconstraints, neural mechanisms, andso on. This asymmetry in the ease ofmaking predictions, combined withthe admitted importance of the hardto-predict factors, leads to properunderstanding of the adaptationistprogram [26]. It is not a claim thateverything is adaptive, but an effectivemethod of scientific inquiry thatbegins with an adaptationist hypothesisas the best first guess, with the fullexpectation that it will be partiallywrong due to the many hard-to-predictfactors. Partial failures are then usedas guide for the identification of otherfactors. This is not the only way toconduct evolutionary science, but Ihave used it as an effective way to orderthe sequence of ideas pedagogically.The Gouldian paradigm does not comefirst, but it does occupy center stagefor a section of the course with theintention of making it a permanentpart of the conceptual framework beingbuilt.Evolutionary adaptations arenot always benign. Even whenorganisms are highly adapted to theirenvironments, their properties donot always correspond to the intuitivenotion of adaptation. Everyone canagree about the impressive design of abutterfly that exactly resembles a leaf,or a fish shaped to cruise effortlesslythough the water, but how about aspecies that degrades its own habitat ora social partner who fails to cooperate?Fitness is a relative and local concept.It doesn’t matter how well an organismsurvives and reproduces, only that itdoes so better than other organismsin its vicinity. As a result, manyevolutionary adaptations appear selfishand shortsighted in human terms,creating problems at larger temporaland spatial scales.If behaviors regarded as immoralin human terms are adaptive and“natural,” then aren’t all the fearsabout evolution justified? No—becausebehaviors that are regarded as moralin human terms are also adaptiveand “natural” under the rightcircumstances, which can be illustratedwith the following exercise of the sortsuggested by Nelson and Alters. First,the class is asked to list the behaviorsthat they associate with morality. Themost common items include altruism,honesty, love, charity, sacrifice, loyalty,bravery, and so on. Then they are askedto list behaviors that they associate withimmorality, and respond with oppositeitems such as selfishness, deceit,hatred, miserliness, and cowardice.With these lists in mind, the studentsare asked three questions: (1) Whatwould happen if you put a singlemoral individual and a single immoralindividual together on a desert island?(The students quickly conclude thatthe moral individual would becomeshark food within days.) (2) Whatwould happen if you put a group ofmoral individuals on one island anda group of immoral individuals onanother island? (The students areequally quick to conclude that the1004December 2005 Volume 3 Issue 12 e364

Table 1. A Sample of Speakers in the Campus-Wide EvoS Seminar Series during the 2004–2005 Academic YearSpeakerInstitutionTitle of SeminarLinda BartoshukYale University (New Haven, Connecticut, United States)Ellen DissanayakeDaniel E. DykhuizenAllan GibbardHerbert GintisUniversity of Washington (Seattle, Washington, United States)Stony Brook University (Stony Brook, New York, United States)University of Michigan (Ann Arbor, Michigan, United States)University of Massachusetts (Amherst, Massachusetts, UnitedStates)University of Pittsburgh (Pittsburgh, Pennsylvania, UnitedStates)University of Pennsylvania (Philadelphia, Pennsylvania, UnitedStates)Cornell University (Ithaca, New York, United States)Are you a supertaster? How do we know? What does it mean foryour health?The deep structure of the artsEcology, evolution, and molecular biology of Lyme diseaseMoral emotions and moral conceptsUnity in the behavioral sciencesPaul E. GriffithsRobert KurzbanIrby J. LovetteIan S. LustickDavid B. NewlinMassimo PigluicciPaul RozinHiroki SayamaCharles SpencerThomas G. WhithamUniversity of Pennsylvania (Philadelphia, Pennsylvania, UnitedStates)Research Triangle Institute (Research Triangle Park, NorthCarolina, United States)Stony Brook University (Stony Brook, New York, United States)University of Pennsylvania (United States)University of Electro-communications (Tokyo, Japan)American Museum of Natural History (New York City, New York,United States)Northern Arizona University (Flagstaff, Arizona, United States)Representing genesEvolution, trust, and reciprocityHow to build a warbler: Diversity and diversification in NorthAmerica’s most spectacular avian radiationFrom basic evolutionary theory to applied social science: Thepromise of agent-based modelingThe self-perceived survival ability and reproductive fitness theoryof substance abuse disordersLost in phenotypic space: Why do living organisms look the waythey do?Pre-adaptation and the cultural evolution of disgustEvolutionary dynamics of spatially extended population modelsThe evolution of a primary state in ancient OaxacaCommunity and ecosystem genetics: A consequence of extendedphenotypesDOI: 10.1371/journal.pbio.0030364.t001moral group would work together toescape the island or turn it into a littleutopia, while the immoral group wouldself-destruct.) (3) What would happenif you allow one immoral individualto paddle over to Virtue Island? (Theanswer to this question is complexbecause it is a messy combination of thestraightforward answers to the first twoquestions.)This exercise is simple andentertaining, but profound in itsimplications. It shows that most of thetraits associated with human moralitycan be biologically adaptive. Groups ofmoral individuals are likely to surviveand reproduce better than any otherkind of group. The problem withmorality is its vulnerability to subversionfrom within. To the extent that naturalselection is based on fitness differenceswithin groups, behaviors associatedwith immorality are the expectedoutcome. To the extent that naturalselection is based on fitness differencesamong groups, behaviors associatedwith morality are the expectedoutcome (these statements apply to allevolutionary models of cooperationand altruism when the relevant groupsare appropriately defined, includinginclusive fitness theory, evolutionarygame theory, and multilevel selectionPLoS Biology www.plosbiology.orgtheory) [27,28]. The discerningstudent quickly perceives a disturbingcorollary: Can’t behaviors that countas moral within groups be used forimmoral purposes among groups? Theanswer to this question is “yes,” whichmeans that moral conduct amonggroups is a different and more difficultevolutionary problem to solve thanmoral conduct within groups [14,27].The important point is thatevolutionary theory can potentiallyexplain the evolution of behaviorsassociated with morality andimmorality. This is vastly differentthan the usual portrayal of evolutionas a theory that explains immoralitybut leaves morality unaccounted for.The average student is well aware thatimmoral behaviors usually benefitthe actor, that human groups have adisturbing tendency to confine moralconduct to their own members, andso on. When evolutionary theoryis presented as a framework forunderstanding these patterns in alltheir complexity, including the good,the bad, the beautiful, and the ugly, itis perceived as a tool for understandingthat can be used for positive ends,rather than as a threat. These issuesare discussed in more detail later inthe course. In the initial sequence ofideas, it is important to establish thatevolutionary adaptations are not alwaysadaptive in the everyday sense of theword, and that societal adaptations inparticular require special conditions toevolve.Using the framework. At this point(about mid-semester), the studentsare told that they have acquired aconceptual framework that can beused to study virtually any subject inbiology and human affairs, whichwill be used to study particular topicsfor the rest of the semester. Thereis great flexibility in the topics thatcan be chosen, which is facilitated byhaving the students read, rather thana textbook, well-chosen articles fromthe primary scientific literature. I beginwith the subject of Darwinian medicine;it is intrinsically interesting, illustratesa number of general principles, and isdirectly relevant to students preparingfor careers in the health sciences.The health sciences are enormouslysophisticated in the study of proximatemechanisms but often ignorant ofevolutionary principles, as pointedout by G.C. Williams and R. Nessein their influential scientific article,“The Dawn of Darwinian Medicine”[29] and popular book Why We GetSick [30]. Simply put, most

university-wide program. It is based on a campus-wide evolutionary studies program called EvoS (http: bingweb. binghamton.edu/ evos/), initiated at Binghamton University in 2002, which currently includes over 50 faculty members representing 15 departments. E