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Behavioral Ecology (2014), 00(00), 1–5. doi:10.1093/beheco/aru079

The official journal of the

ISBEInternational Society for Behavioral Ecology

Behavioral Ecology

Anniversary Essay

The past and the future of Behavioral EcologyManfred MilinskiDepartment of Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, Thienemann-Strasse 2, 24306 Plön, GermanyReceived 6 April 2014; accepted 8 April 2014.

The design of brains, sense organs, or immune systems is an impressive product of natural selection, far ahead of human engineer-ing capability. But what if behavior is less well adapted? A bird’s perfect eye is useless if it fails to avoid a stalking cat. If we fail in choosing a partner with complementary immunogenes, our ability to detect major histocompatibility complex–dependent body odors is worthless. Besides being able to detect all available prey items, the diet that maximizes net energy gain must be chosen. Individuals that are selected naturally will be those best able to avoid predators, choose mates, select food, and so on. Those with less perfect behavior produce fewer offspring, and their genotypes will disappear. Ecology is the stage on which the fittest have behaved most suc-cessfully. Thus, their strategies prevail today. Behavioral ecology is about the optimal design of behavior.

Key words : future, history, manipulation, multiple infection, parasite personalities.

Of Tinbergen’s (1951) 4 questions, we concentrate on studying the selective forces that have shaped the evolution of a behavior. Good old Lorenzian Ethology (Eibl-Eibesfeldt 1970) that I was taught as a student studied the phylogeny and causation, or mechanisms, of behavior. I  was both impressed and bewildered to hear that ani-mals are like robots; when a certain subprogram, for example, motivation to feed young, is switched on, their IRM (innate releas-ing mechanism) reacts to the stimulus, gape of a chick, even if the reaction does not make sense, for example, when the gape is a dummy. Parent birds prefer to feed the larger gape of begging nest-lings even if this is a begging cuckoo, 3 times bigger than the feed-ing bird. When I asked “how can the feeding bird be so stupid,” my professor said, it prefers the stronger or supernormal stimulus. And any behavior was said to have evolved to propagate the species. Why then should little birds feed gigantic cuckoo chicks? I  found the textbook wisdom of that time unconvincing.

Even though there were fantastic studies exploring experimen-tally the mechanisms, the software of behavior as Baerends (1976) called it, it appeared to me as studying the syntax of a foreign lan-guage of which I do not understand a word. The arrival of a new discipline that studied how a behavior solves a request from ecol-ogy in a way that increases the actor’s fitness raised great expec-tations—behavioral ecology offered a way of finding the meaning of the “words.” This approach had been known for morphological adaptations: If ecology requests the ability to see pictures, a cam-era eye is the best solution. Both vertebrates and the ancestors of

octopus evolved it independently to similar perfection. Behavioral ecology applies the same philosophy to understand the adaptation of behavior that evolved for the good of the individual, not for the good of the species. Traits “for the good of the group” can evolve; however, the conditions are extremely restrictive, and I  think not fulfilled by any species (Kilmer and Levin 1974; Traulsen and Nowak 2006).

Behavioral ecology had many roots. For example, Tinbergen (1949) found, with numerous versions of a dummy gull’s head on which he varied color and position of the naturally red dot on the beak, that chicks peck at and are thus directed to the right position to collect the food that is regurgitated on the chick’s pecking, per-fect communication. The breakthrough for behavioral ecology came with the idea that behavior has been selected to be efficient. Among others Schoener (1971) applied principles from economics to pre-dict the optimal diet that maximizes the animal’s rate of net energy intake when several types of prey differ in energy content, handling, and search time. Predictions appeared counterintuitive: when the search time for the most profitable prey type is below a threshold, the animal should eat only this type and ignore all others; above the threshold, it eats each type on encounter. Two elegant experi-mental studies, on great tits (Krebs et al. 1977) and bluegill sunfish (Werner and Hall 1974), found strong support for this prediction. Now the door was open to expect economic behavior everywhere: when exploiting patchy food, the marginal value theory (Charnov 1976; Parker and Stuart 1976) predicts the best strategy, and star-lings use it (Kacelnik 1984); when competing for patchy food, ideal free theory offers the best behavior (Fretwell and Lucas 1970), and sticklebacks use it (Milinski 1979). Frightening but impressive: little Address correspondence to M. Milinski. E-mail: milinski@evolbio.mpg.de.

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birds go for a 50% chance of death (or 50% chance of survival) by preferring a highly to a less variable source of food when the average gain is the same for both but not enough to survive the night (Caraco et  al. 1980). “Optimal foraging” was the bandwagon for a decade. Every behavior seemed to be optimally designed, and if not, optimal sampling leads to optimal diet choice (Krebs et  al. 1977), or forag-ing maximally was traded off with avoiding predation at the same time with more weight given to the more burning need (Milinski and Heller 1978). A  long period of detailed studies on foraging strate-gies followed, from which the newly founded journal “Behavioral Ecology” received its first big push and continuous flow of papers.

Sexual selection and mate choice comprised the next bandwagon, again kicked off by new ground breaking theory. Since Darwin (1871) admitted that secondary sexual ornaments, usually of males, chal-lenged his theory of evolution by natural selection, numerous evo-lutionary biologists have tried to solve this puzzle. How can a female preference for “handicapped” fathers (e.g., Andersson 1982) of her offspring evolve? This phenomenon, for which the peacock’s tail—actually its “train”—is a metaphor, is so obvious and so widespread that it seemed to question the evolutionary approach in general. Fisher’s (1930) runaway process solved the puzzle as he saw it, but nobody understood. Against his habits, he did not prove his idea mathematically because “it was easy to see.” It took 50  years until Lande (1981) proved Fisher right with a complex mathematical model. Not much empirical evidence for this “bad genes” model has been provided (Bakker 1993; Wilkinson and Reillo 1994). At the same time, Hamilton and Zuk (1982) offered a new “good genes” theory that made up for problems (Maynard Smith 1976, 1978) of Zahavi’s (1975) handicap principle. Hamilton and Zuk assumed that females need to select the males that carry genes for resistance against the currently prevailing disease. Instead of doing a medical health test, they prefer the male that can afford to display long feathers, bright colors, loud songs, and energetic dances—this male must be healthy and thus most probably carries the needed immunogene. In this way, female choice ensures that most of the next generation will carry this good gene, and the prevailing disease disappears. Now another disease can spread for which another gene for resistance is needed, again revealed by displaying the same kind of costly ornament. This Red Queen dynamic (Van Valen 1973; Lively and Dybdahl 2000) guarantees that neither a resistance gene nor an infectious disease can go to fixation. Although the assumed polymorphic genes for resistance were unknown, the first wave of experimental studies con-firmed a number of assumptions and predictions of the Hamilton-Zuk model (Milinski and Bakker 1990; Møller 1990; Zuk et al. 1990), further waves followed with neat experimental studies—behavioral ecology at its best. Darwin’s puzzle seemed to be solved.

The nature of the “good” resistance genes was still elusive. Several studies with inbred strains of mice found that they prefer the smell of potential partners that differed more in their polymor-phic MHC (major histocompatibility complex) immune genes (e.g., Yamazaki et al. 1976). T-shirt tests (Wedekind et al. 1995) revealed the same preference in humans. Now MHC-related mate choice became a sub-bandwagon of sexual selection in behavioral ecology, a bandwagon that is still moving.

We now know that mate choice goes for achieving optimally rather than maximally MHC heterozygous offspring (Wegner et al. 2003, see Milinski 2006 for review), we even choose our perfume such that it amplifies our individual MHC odor signal (Milinski and Wedekind 2001). The most recent step was to synthesize the MHC odor signal and to show that it predictably functions during mate choice experiments; it is the same molecule in mice (Leinders-Zufall et al. 2004), sticklebacks (Milinski et al. 2005), and humans

(Milinski et al. 2013). Now our individual natural perfume can be synthesized. MHC-dependent mate choice has 2 steps: smell out from a distance the partner that offers the optimally complemen-tary number of MHC alleles to yours, among those select the one with the most expressed (costly) ornament guaranteeing that his/her complementary alleles contain the one that provides resistance against the current infectious disease. The Hamilton and Zuk “good genes” are in fact MHC genes at least in vertebrates (Eizaguirre et al. 2012). The journal Behavioral Ecology was born when the sexual selection wave was on its ascent. It has been a great time for study-ing the function of mate choice and for our journal.

In evolutionary arms races between hosts and parasites, pro-tagonists need “all the running you can do to keep in the same place” as Lewis Carroll’s (1872) Red Queen says in “Through the Looking Glass.” This is illustrated by revolutionary results of “Red Queen coevolution” between cuckoos and their hosts (e.g., Wynne-Edwards 1933), especially so by the beautiful experimental work of Nick Davies and his school over the past 25 years (e.g., Davies and Brooke 1988; Kilner et  al. 1999; Kilner and Langmore 2011; see Davies 2011 for a review). They uncovered the evolution of tricks and counter-tricks of almost unbelievable creativity—traits that must have started as mutations without limits for inventions.

Why invest to increase another individual’s fitness? Understanding cooperation and altruism through kin selection is a cornerstone of behavioral ecology. Already Fisher (1930) explained the distastefulness of some caterpillars with the preda-tor’s reluctance to eat the nearby brothers and sisters of the dis-tasteful victim. They survive and share each gene of the victim with 50% probability as Fisher mentioned. He also recognized that in distasteful species, the mother deposits her eggs in clumps, whereas tasty butterflies lay only 1 egg per plant. The conditions for the spread of an altruistic behavior toward relatives are given by Hamilton’s rule: the benefit to cost ratio must be greater than 1 divided by the relatedness of the altruist to the recipient. With relatedness of half between full siblings, the benefit must be at least twice the cost. Hamilton (1964) showed that especially worker altruism in hymenoptera with their haplodiploid sex determination is nicely explained with kin selection. This solution was criticized by Alexander (1974) who argued that it is not kin selected altruism by the workers but simply manipulation by the queen. Trivers and Hare (1976) disproved the manipulation hypothesis with their ele-gant test showing that the Fisher (1930) sex ratio of investment in male and female reproductives is not 1:1 according to the Queen’s interests but 3:1 (in favor of young queens), which is in the work-ers’ interest. Kin selection theory triumphed. Later Ratnieks and Visscher (1989) showed that indeed the workers’ policing removes “unwanted” males. Numerous studies assembled an impres-sive body of complex and consistent evidence for kin selection, or inclusive fitness theory, driving a large part of social behavior (review for ants, Hölldobler and Wilson 2008), beyond any doubt as it seemed. However, Nowak et al. (2010) criticized the theoreti-cal basis of Hamilton’s rule and claimed that there are no exam-ples that can be explained by the rule. The “empire struck back” (Abbot et  al. 2011), 139 authors refuting the criticism of Nowak et  al. completely. I  am not involved in this dispute, but I have an opinion: both sides have a point. Already van Veelen (2005) and van Veelen et  al. (2012) had provided a mathematical proof that the Price Equation, on which inclusive fitness theory is based, can-not serve as its foundation. On the other hand, our complex and consistent knowledge of kin-related cooperation is based on over-whelming experimental evidence. My hope is that a new well-based theory of kin-related altruism is developed providing a new version

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of Hamilton’s rule, which, I bet, will not be too different from the previous one. New, then well-based, predictions will keep the next generation of behavioral ecologists busy testing them—and we will understand social behavior better.

For cooperation based on direct reciprocity (Trivers 1971; Axelrod and Hamilton 1981), relatedness is neither a prerequisite nor a hin-drance. The iterated Prisoner’s Dilemma is the basic model. I help you, and you help me (hopefully) later, helping costs less than the receiver gains, we both have a net gain. Nice but retaliatory, Tit for Tat–like strategies (Axelrod 1984; Nowak and Sigmund 1994) had been the predicted champions for 25 years, but see Press and Dyson (2012)for a recent change. Initial experimental support in vampire bats (Wilkinson 1984) and sticklebacks (Milinski 1987) was criticized, I  think mainly because the needed cognitive ability was thought to be too demanding for nonhuman animals. Today, these find-ings have been confirmed (e.g., Ward et al. 2002; Croft et al 2006; Carter and Wilkinson 2013); black hamlet hermaphrodites take turns in spawning eggs in batches to reduce the partner’s defection; “parceling” as Fischer (1980) called it, a phenomenon recently pre-dicted by theory (Johnstone et al. 2014). Mobbing birds (e.g., Krams et al. 2008) and even bacteria have been shown to cooperate (e.g., Rainey and Rainey 2003). Cooperators and defectors show up in experimental evolution studies under the eyes of the experimenter in fungi (Fiegna et al. 2006). Cooperation based on direct reciproc-ity or indirect reciprocity—I help those who have a reputation for helping others (Nowak and Sigmund 1998; Wedekind and Milinski 2000)—is thought to be the dominating driver of cooperation in humans. Here, experimental economists dominate the field (Fehr and Fischbacher 2003), their “homo economicus” has been equiva-lent to a fitness maximizer; we speak the same language it seems (e.g., Rockenbach and Milinski 2006). However, this individual selec-tion–based approach is increasingly giving way to a more group selection–based philosophy among economists, despite being at vari-ance with evolutionary theory (Traulsen and Nowak 2006). Cultural group selection is the yet unproved hypothesis.

What about the future of behavioral ecology? We have prof-ited from new technologies in other fields that helped solve long standing puzzles, for example, radio tracking of migrating birds or even butterflies (e.g., Holland et al. 2006), or DNA finger printing (Jeffreys et al. 1985), which led even to a new technical term such as “EPC” (extrapair copulation). Mating strategies and their con-sequences can be tracked precisely to the neighbors’ clutches even in humans. Even cryptic postcopulatory female choice is no longer cryptic to the experimenter and has proved to be an efficient means of the female to sort several males’ sperm to her advantage (e.g., Olsson et  al. 1996; Wedell et  al. 2002; Simmons and Fitzpatrick 2012). The study of sperm competition boosted by theory pio-neered by Geoff Parker (e.g., Parker 1970) has become very effi-cient. Are these breakthroughs the first signs that also behavioral ecology will inevitably go “omics”? When I  left for Switzerland in 1987, my former dean told me “also you behavior people will do only molecular work 20 years from now.” He has been wrong.

To me, genomics and behavioral ecology appear to be 2 par-allel worlds with little connection. In genomics, whole genomes can be sequenced now for affordable costs, and all the relations among genes, even the time when they showed up, can be precisely determined. However, the phenotype of the majority of genes is unknown, reminding me again of studying the syntax of a for-eign language without understanding the meaning of the words. When a new gene showed up a few thousand years ago, the selec-tion supporting it cannot be even guessed if the gene’s phenotype is unknown. Behavioral ecologists study phenotypes and their relation

to the ecology that made them evolve. We can study all the impres-sive interactions among phenotypes and show in which way they make evolutionary sense. We can even prove that traits have a genetic basis by showing that experimental selection can change the phenotype over generations or by testing naive offspring, for exam-ple, to see if their preferred migration direction resembles that of their parents. Peter Berthold proved with his ingenious and simple techniques that blackcaps from southern Germany have evolved a new migration route to England, which, thanks to climate change, has become more profitable than the old migration route to Spain (Berthold et al. 1992), to which, as he showed, naive offspring from more southern populations still migrate. So, there are genetic differ-ences between these neighbor populations of blackcaps, but there is virtually no way to find the genes that determine the 2 migration directions. Would we understand more if we knew that the respon-sible genes were xy1 and xy2?

There are rare bridges between the genomic and the phenotypic worlds. They can sometimes be goldmines if we can make use of them. MHC immunogenes are one example. We can type them for each individual and know their phenotype, not just their function in the adaptive immune response, but also their role in mate choice, in signaling via odor an individual’s MHC type and in choosing among signalers the sender that offers MHC alleles most comple-mentary to one’s own alleles (see above). There is even more to MHC genes: they also seem to form human facial physiognomy (Roberts et al. 2005; Lie et al. 2008), a fascinating perspective for future research. Although MHC researchers, including myself, make use of MHC as a “bridge gene,” we can hardly enforce find-ing new bridges. In my view, the 2 worlds will remain parallel for a long time. A difference between populations in a specific gene that correlates with, say social behavior, is just “correlational evidence” from which a causal relationship between that gene and the speci-fied social behavior cannot be concluded (Milinski 1997). And yet many such correlations are published as great insights. A  conclu-sive experimental proof is almost impossible to provide. We should apply genomics only if it helps us to solve our particular research problem.

Studying animal personalities, or persisting individual differ-ences in behavior, has become a major fashion. There had been many parallel sessions on “personality” at recent International Society for Behavioral Ecology conferences in Perth 2010 with an additional satellite symposium. The wheel is being reinvented. Felicity Huntingford showed already in 1976 that male stickle-backs that are aggressive toward conspecifics are also persistently bold toward predators, others are persistently both timid and cau-tious (Huntingford 1976). Later “personality,” the term was not yet coined, came under the name “behavioral syndromes” (Sih et  al. 2004). Perhaps the term “behavioral syndromes” was too cryp-tic for the bandwagon to gather speed. I have been to many per-sonality talks. Researchers usually prove that persisting individual differences indeed exist and find consequences, I  was tempted to say, however, actually only correlations with group behavior. No consequences or effects can be concluded from correlational evi-dence because proving a causal relationship requires experimental evidence (Milinski 1997). Researchers rarely ask (e.g., Kortet et al. 2010) how does his/her personality contribute to the actor’s fitness? Does A gain more from having personality a than from having b, and does B gain more from having b instead of a? Designing an experimental test would be challenging, traps are obvious. I  look forward to seeing the result, which would be a breakthrough.

Are there any great challenges for behavioral ecologists ahead that we already know? Virtually no animals and plants would have

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evolved, had they not been forced to reproduce sexually to offset the negative effects of infectious diseases. In a world without infec-tious diseases, asexual reproduction would, indeed, be the pre-vailing reproductive mode (Hamilton et  al. 1990) because it is at least twice as efficient as sexual reproduction (reviews in Maynard Smith 1976; Ridley 2004). However, with asexual reproduction, there is no evolutionary improvement, but only genetic degenera-tion through fatal mutation accumulation, Muller’s ratchet (Muller 1964) clicking inevitably to decline (Maynard Smith 1978, 1990). The only way to stop the ratchet is sexual reproduction removing a new mutation with a probability of 50% per offspring. However, the need to stop Muller’s ratchet does not provide a sufficiently large benefit to override the 2-fold efficiency advantage per gen-eration of asexual reproduction, it is too slow. Kondrachov’s (1988) hypothesis of “synergistic epistasis” of multiple slightly deleterious mutations providing a 2-fold gain per generation (Ridley 2004) has been disproved (e.g., Bonhoeffer et  al. 2004), leaving arms races between hosts and infectious diseases as the only viable mechanism for the evolution of sex and thus organismal diversity.

Thus, parasites are the drivers of evolution. Infectious diseases not only occur in large numbers of species but also in a large num-ber of individuals per species, and they change permanently across space and time. Optimizing offspring resistance in each generation anew, the primary function of mate choice, offers a sufficiently high short-term advantage for sex to evolve and be maintained. Besides parasite selection on mate choice, there are puzzling gaps and burning questions in our knowledge of how pathogens drive host evolution and vice versa.

It is textbook knowledge (e.g., Moore 2002) that some parasites manipulate the behavior of their hosts to enhance the probability of transmission to the next host. There is also counter-manipulation before the time window of transmission has been reached (Koella et al. 2002; Hammerschmidt et al. 2009; Diane et al. 2011); thus, hosts may always be manipulated. Human toxoplasmosis with a worldwide prevalence of about 30% is supposed to permanently manipulate the behavior of infected people and is probably responsible for hundreds of thousands of deaths due to its effects on the rate of traffic and workplace accidents and also suicides (Flegr 2013). This is not the host’s personality. If anything, it is the personality of the manipulating parasite, its extended phenotype as Dawkins would call it. Parasites of the same species, some already resident and others newly arriv-ing within the time window of the residents’ transmission, are in conflict over manipulating the host’s behavior—competing parasite personalities. Who wins the conflict? Under natural conditions, hosts are parasitized by several parasites of different species simultaneously, for example, parasites of up to 12 different species have been found in wild caught sticklebacks (Kalbe M, personal communication). Even parasites that are happy with their host’s normal behavior are expected to interfere if any other parasite starts manipulating. What we know about parasite manipulation appears to me as the tip of the iceberg. Multiple parasite manipulation might be a topic for the near future. The interest of the host comes last as it seems.

Editor-in-Chief: Leigh Simmons

RefeRencesAbbot P, Abe J, Alcock J, Alizon S, Alpedrinha JAC, Andersson M, Andre

J-B, van Baalen M, Balloux F, Balshine S, et  al. 2011. Inclusive fitness theory and eusociality. Nature. 471:E1–E2.

Alexander RD. 1974. The evolution of social behavior. Annu Rev Ecol Syst. 5:325–383.

Andersson M. 1982. Female choice selects for extreme tail length in a wid-owbird. Nature. 299:818–820.

Axelrod R. 1984. The evolution of cooperation. New York: Basic Books.Axelrod R, Hamilton WD. 1981. The evolution of cooperation. Science.

211:1390–1396.Baerends GP. 1976. Functional organization of behavior. Anim Behav.

24:726–738.Bakker TCM. 1993. Positive genetic correlation between female preference

and preferred male ornament in sticklebacks. Nature. 363:255–257.Berthold P, Helbig AJ, Mohr G, Querner U. 1992. Rapid microevolution of

migratory behaviour in awild bird species. Nature. 360:668–670.Bonhoeffer S, Chappey C, Parkin NT, Whitcomb JM, Petropoulos

CJ. 2004. Evidence for positive epistasis in HIV-1. Science. 306:1547–1550.

Caraco T, Martindale S, Whitham TS. 1980. An empirical demonstration of risk-sensitive foraging preferences. Anim Behav. 28:820–830.

Carroll L. 1872. Through the looking glass. London: MacMillan.Carter GG, Wilkinson GS. 2013. Food sharing in vampire bats: reciprocal

help predicts donations more than relatedness or harassment. Proc R Soc Lond B. 280:1–6.

Charnov EL. 1976. Optimal foraging: the marginal value theorem. Theor Popul Biol. 9:129–136.

Croft DP, James R, Thomas POR, Hathaway C, Mawdsley D, Laland KN, Krause J. 2006. Social structure and co-operative interactions in a wild population of guppies (Poecilia reticulata). Behav Ecol Sociobiol. 59:644–650.

Darwin C. 1871. The descent of man and selection in relation to sex. London: John Murray.

Davies NB. 2011. Cuckoo adaptations: trickery and tuning. J Zool. 284:1–14.Davies NB, Brooke MdeL. 1988. Cuckoos versus reed-warblers. Adaptations

and counteradaptations. Anim Behav. 36:262–284.Diane L, Perrot-Minnot MJ, Bauer A. 2011. Protection first then facilita-

tion: a manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution. 65:2692–2698.

Eibl-Eibesfeldt I. 1970. Grundriß der vergleichenden Verhaltensforschung. München (Germany): Piper Verlag.

Eizaguirre C, Lenz TL, Kalbe M, Milinski M. 2012. Rapid and adaptive evolution of MHC genes under parasite selection in experimental verte-brate populations. Nat Commun. 3:621.

Fehr E, Fischbacher U. 2003. The nature of human altruism. Nature. 425:785–791.

Fiegna F, Yu YTN, Kadam SV, Velicer GJ. 2006. Evolution of an obligate social cheater to a superior cooperator. Nature. 441:310–314.

Fischer EA. 1980. The relationship between mating system and simul-taneous hermaphroditism in the coral reef fish, Hypoplectrus nigricans (Serranidae). Anim Behav. 28:620–633.

Fisher RA. 1930. The genetical theory of natural selection. Oxford: Oxford University Press.

Flegr J. 2013. How and why Toxoplasma makes us crazy. Trends Parasitol. 29:156–163.

Fretwell SD, Lucas HL Jr. 1970. On territorial behavior and other factors influencing habitat distribution in birds. Acta Biotheor. 19:16–36.

Hamilton WD. 1964. The genetical evolution of social behaviour. J Theor Biol. 7:1–52.

Hamilton WD, Axelrod R, Tenese R. 1990. Sexual reproduction as an adap-tation to resist parasites (a review). Proc Natl Acad Sci USA. 87:3566–3573.

Hamilton WD, Zuk M. 1982. Heritable true fitness and bright birds: a role for parasites? Science. 218:384–387.

Hammerschmidt K, Koch K, Milinski M, Chubb JC, Parker GA. 2009. When to go: optimization of host switching in parasites with complex life cycles. Evolution. 63:1976–1986.

Holland RA, Wikelski M, Wilcove DS. 2006. How and why do insects migrate? Science. 313:794–796.

Hölldobler B, Wilson EO. 2008. The superorganism: the beauty, ele-gance, and strangeness of insect societies. New York: W. W. Norton and Company. pp. 522.

Huntingford FA. 1976. The relationship between anti-predator behav-iour and aggression among conspecifics in the three-spined stickleback, Gasterosteus aculeatus. Anim Behav. 24:245–260.

Jeffreys AJ, Wilson V, Thein SL. 1985. Hypervariable minisatellite regions in human DNA. Nature. 314:67–73.

Johnstone RA, Manica A, Fayet AL, Stoddard MC, Rodriguez-Gironés, MA, Hinde CA. 2014. Reciprocity and conditional cooperation between great tit parents. Behav Ecol. 25:216–222.

Page 4 of 5

at Universidade Federal do R

io Grande do N

orte on May 26, 2014

http://beheco.oxfordjournals.org/D

ownloaded from

Milinski • The past and the future of behavioral ecology

Kacelnik A. 1984. Central place foraging in starlings (Sturnus vulgaris). I. Patch residence time. J Anim Ecol. 53:283–299.

Kilmer WL, Levin BR. 1974. Interdemic selection and evolution of altru-ism—computer-simulation study. Evolution. 28:527–545.

Kilner RM, Langmore NE. 2011. Cuckoos versus hosts in insects and birds: adaptations, counteradaptations and outcomes. Biol Rev. 86:836–852.

Kilner RM, Noble DG, Davies NB. 1999. Signals of need in parent-off-spring communication and their exploitation by the common cuckoo. Nature. 397:667–672.

Koella JC, Rieu L, Paul REL. 2002. Stage-specific manipulation of a mos-quito’s host-seeking behavior by the malaria parasite Plasmodium gallina-ceum. Behav Ecol. 13:816–820.

Kondrachov AS. 1988. Deleterious mutations and the evolution of sexual reproduction. Nature. 336:435–440.

Kortet R, Hedrick AV, Vainika A. 2010. Parasitism, predation and the evo-lution of animal personalities. Ecol Lett. 13:1449–1458.

Krams I, Krama T, Igaune K, Mand R. 2008. Experimental evidence of reciprocal altruism in the pied flycatcher. Behav Ecol Sociobiol. 62:599–605.

Krebs JR, Erichsen JT, Webber MI, Charnov EL. 1977. Optimal prey selec-tion in the great tit, Parus major. Anim Behav. 25:30–38.

Lande R. 1981. Models of speciation by sexual selection on polygenic traits. Proc Natl Acad Sci USA. 78:3721–3725.

Leinders-Zufall T, Brennan P, Widmayer P, Chandramani P, Maul-Pavicic A, Jager M, Li XH, Breer H, Zufall F, Boehm T. 2004. MHC class I peptides as chemosensory signals in the vomeronasal organ. Science. 306:1033–1037.

Lie HC, Rhodes G, Simmons LW. 2008. Genetic diversity revealed in human faces. Evolution. 62:2473–2486.

Lively CM, Dybdahl MF. 2000. Parasite adaptation to locally common host genotypes. Nature. 405:679–681.

Maynard Smith J. 1976. Sexual selection and the handicap principle. J Theor Biol. 57:239–242.

Maynard Smith J. 1978. The evolution of sex. Cambridge (UK): Cambridge University Press.

Maynard Smith J. 1990. Clicking into decline? Nature. 348:391–392.Milinski M. 1979. An evolutionarily stable feeding strategy in sticklebacks.

Z Tierpsychol. 51:36–40.Milinski M. 1987. TIT FOR TAT and the evolution of cooperation.

Nature. 325:433–435.Milinski M. 1997. How to avoid seven deadly sins in the study of behavior.

Adv Study Behav. 26:159–180.Milinski M. 2006. The major histocompatibility complex, sexual selection,

and mate choice. Annu Rev Ecol Evol Syst. 37:159–186.Milinski M, Bakker TCM. 1990. Female sticklebacks use male coloration

in mate choice and hence avoid parasitised males as mates. Nature. 344:330–333.

Milinski M, Croy I, Hummel T, Boehm T. 2013. Major histocompatibility complex peptide ligands as olfactory cues in human body odour assess-ment. Proc R Soc Lond B. 280:1–7.

Milinski M, Griffiths S, Wegner KM, Reusch TBH, Haas-Assenbaum A, Boehm T. 2005. Mate choice decisions of stickleback females pre-dictably modified by MHC peptide ligands. Proc Natl Acad Sci USA. 102:4414–4418.

Milinski M, Heller R. 1978. Influence of a predator on the optimal forag-ing behaviour of sticklebacks (Gasterosteus aculeatus). Nature. 275:642–644.

Milinski M, Wedekind W. 2001. Evidence for MHC-correlated perfume preferences in humans. Behav Ecol. 12:140–149.

Møller AP. 1990. Effects of a haematophagous mite on the barn swallow (Hirundo rustica): a test of the Hamilton and Zuk hypothesis. Evolution. 44:771–874.

Moore J. 2002. Parasites and the behavior of animals. Oxford: Oxford University Press.

Muller HJ. 1964. The relation of recombination to mutational advance. Mutat Res. 1:2–9.

Nowak MA, Sigmund K. 1994. A strategy of win-stay, lose-shift that out-performs tit-for-tat in the Prisoner’s Dilemma. Nature. 364:56–58.

Nowak MA, Sigmund K. 1998. Evolution of indirect reciprocity by image scoring. Nature. 393:573–577.

Nowak MA, Tarnita CE, Wilson EO. 2010. The evolution of eusociality. Nature. 466:1057–1062.

Olsson M, Shine R, Madsen T, Gullberg A, Tegelström H. 1996. Sperm selection by females. Nature. 383:585.

Parker GA. 1970. Sperm competition and its evolutionary consequences in insects. Biol Rev. 45:525–567.

Parker GA, Stuart RA. 1976. Animal behavior as a strategy optimizer: evo-lution of resource assessment strategies and optimal emigration thresh-olds. Amer Natur. 110:1055–1076.

Press WH, Dyson FJ. 2012. Iterated Prisoner’s Dilemma contains strate-gies that dominate any evolutionary opponent. Proc Natl Acad Sci USA. 109:10409–10413.

Rainey PB, Rainey K. 2003. Evolution of cooperation and conflict in experimental bacterial populations. Nature. 425:72–74.

Ratnieks FLW, Visscher PK. 1989. Worker policing in the honeybee. Nature. 342:796–797.

Ridley M. 2004. Evolution. 3rd ed. Oxford: Blackwell.Roberts SC, Little AC, Gosling LM, Perrett DI, Carter V, Jones BC,

Penton-Voak I, Petrie M. 2005. MHC-heterozygosity and human facial attractiveness. Evol Hum Behav. 26:213–226.

Rockenbach B, Milinski M. 2006. The efficient interaction of indirect reci-procity and costly punishment. Nature. 444:718–723.

Schoener TW. 1971. Theory of feeding strategies. Annu Rev Ecol Syst. 2:369–404.

Sih A, Bell A, Johnson JC. 2004. Behavioural syndromes: an ecological and evolutionary overview. Trends Ecol Evol. 19:372–378.

Simmons LW, Fitzpatrick JL. 2012. Sperm wars and the evolution of fertil-ity. Reproduction. 144:519–534.

Tinbergen N. 1949. De functie van de rode vlek op de snavel van de zilver-meeuw. Bijdragen tot Dierkunde. 28:453–465.

Tinbergen N. 1951. The study of instinct. Oxford: Clarendon Press.Traulsen A, Nowak MA. 2006. Evolution of cooperation by multilevel

selection. Proc Natl Acad Sci USA. 103:10952–10955.Trivers RL. 1971. The evolution of reciprocal altruism. Q Rev Biol.

46:35–57.Trivers RL, Hare H. 1976. Haplodiploidy and evolution of social insects.

Science. 191:249–263.Van Valen L. 1973. A new evolutionary law. Evol Theory. 3:1–30.van Veelen M. 2005. On the use of the Price equation. J Theor Biol.

237:412–426.van Veelen M, García J, Sabelis MW, Egas M. 2012. Group selection and

inclusive fitness are not equivalent; the Price equation vs. models and sta-tistics. J Theor Biol. 299:64–80.

Ward AJ, Botham MS, Hoare DJ, James R, Broom M, Godin JG, Krause J. 2002. Association patterns and shoal fidelity in the three-spined stickle-back. Proc R Soc Lond B. 269:2451–2455.

Wedekind C, Milinski M. 2000. Cooperation through image scoring in humans. Science. 288:850–852.

Wedekind C, Seebeck T, Bettens F, Paepke AJ. 1995. MHC-dependent mate preferences in humans. Proc R Soc Lond B. 260:245–249.

Wedell N, Gage MJG, Parker GA. 2002. Sperm competition, male pru-dence and sperm limited females. Trends Ecol Evol. 17:313–320.

Wegner KM, Kalbe M, Kurtz J, Reusch TBH, Milinski M. 2003. Parasite selection for immunogenetic optimality. Science. 301:1343.

Werner EE, Hall DJ. 1974. Optimal foraging and the size selection of prey by bluegill sunfish (Lepomis macrochirus). Ecology. 55:1042–1052.

Wilkinson GS. 1984. Reciprocal food sharing in the vampire bat. Nature. 308:181–184.

Wilkinson GS, Reillo PR. 1994. Female choice response to artificial selec-tion on an exaggerated male trait in a stalk-eyed fly. Proc R Soc Lond B. 255:1–6.

Wynne-Edwards VC. 1933. Inheritance of egg-colour in the ‘parasitic’ cuckoos. Nature. 132:822.

Yamazaki K, Boyes EA, Thaler HT, Mathieson BJ, Abbott J, Boyes J, Zayas ZA. 1976. Control of mating preferences in mice by genes in the major histocompatibility complex. J Exp Med. 144:1324–1335.

Zahavi A. 1975. Mate selection: a selection for a handicap. J Theor Biol. 53:205–214.

Zuk M, Thornhill R, Ligon JD. 1990. Parasites and mate choice in red jun-gle fowl. Am Zool. 30:235–344.

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