Neuroscience and Biobehavioral Reviews 46 (2014) 501–508 Contents lists available at ScienceDirect Neuroscience and Biobehavioral Reviews jou rn al h om epage: www.elsev ier .com/ locate /neubiorev Review Darwin Mary Jan Smithsonian Tr Biología, Unive a r t i c l Article history: Received 13 Fe Received in re Accepted 27 Ju Available onlin Keywords: Social selectio Sexual conflict Good genes Sensory bias Female choice Evolution of communication Threat behavior Sensory systems Evolution of complexity antagonistic co-evolution” of sensory-response systems toward the powerful domain of sexually syner- gistic co-evolution under sexual selection. Special properties of sexual selection apply to other forms of social competition as well, showing the wisdom of Darwin’s setting it apart from natural selection as an explanation of many otherwise puzzling and extreme traits. © 2014 Published by Elsevier Ltd. Contents 1. Introd 2. Darw 3. Darw 4. Specia 4.1. 4.2. 4.3. 4.4. 4.5. 5. When 6. Sexua 6.1. 6.2. 6.3. 6.4. 6.5. 6.6. 7. Concl Ackno Refer ∗ Tel.: +1 22 E-mail add http://dx.doi.o 0149-7634/© uction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 502 in’s distinction between natural selection and sexual selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 502 inian sexual selection as social selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 502 l properties of social selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 503 The unending nature of change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 503 The potential for runaway change under choice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 503 The relentlessness of social selection within and across generations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 503 The very large number of factors and cues that can initiate change in new directions (see West-Eberhard, 1983) . . . . . . . . . . . . . . . . . . . . . . 504 The potential for very large differences in reproductive success . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 504 to suspect that sexual/social selection may be important. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 504 l-selection amnesia and the interplay between natural and sexual selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 504 Natural and sexual selection in signal evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 505 “Good-genes” indicators and the corruption of honest signals by socially-selected noise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 505 Conflict theory, and sexually antagonistic co-evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 505 A conflict-theory paradox and the emergence of sexually synergistic co-evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 506 Post-copulatory sexual selection: sperm competition or female choice? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 507 Sensory exploitation and sensory traps: natural-selection origins of social signals. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 507 usion: natural and sexual selection as causes of neurobiological evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 507 wledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 507 ences . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 507 5 332 3520/506 2228 0001. ress: mjwe@sent.com rg/10.1016/j.neubiorev.2014.06.015 2014 Published by Elsevier Ltd.’s forgotten idea: The social essence of sexual selection e West-Eberhard ∗ opical Research Institute, Louisiana State University Department of Biological Sciences and Museum of Natural Science, c/o Escuela de rsidad de Costa Rica, Ciudad Universitaria, Costa Rica e i n f o bruary 2014 vised form 26 May 2014 ne 2014 e 6 July 2014 n a b s t r a c t Darwinian sexual selection can now be seen in the broader context of social selection, or social competi- tion for resources (under sexual selection, mates or fertilization success). The social-interaction aspects of sexually selected traits give them special evolutionary properties of interest for neurobiological studies of stimulus–response systems because they can account for highly complex systems with little information content other than stimulatory effectiveness per se. But these special properties have a long history of being forgotten when other factors dominate the analysis of male–female interactions, such as the mis- taken belief that differential responsiveness to signals produced by competing rivals (“female choice”) requires an esthetic sense; that species recognition explains all species-specific sexual signals; and, more recently, that successful signals must reflect good survival genes; or that male–female conflict involves female resistance rather than stimulus evaluation. A “conflict paradox” results when male–female con- flict is seen as driven by natural selection, whose costs should often move the hypothesized “sexually 502 M.J. West-Eberhard / Neuroscience and Biobehavioral Reviews 46 (2014) 501–508 1. Introduction Darwin selection. T Selection, is and the se Sex (1871) beginning w Gray that r that defy ex for existen the eye ma structure of in a peacoc Darwin, 189 The peac system who (see Flinn e under stron communica exploits a m than one si collared ma et al, this is trated by B and Beani ( sex-related the special produce co expected un important f in the func such system The neural mosaic patt ical depend social selec caretakers o This issu fresh look a to the evo of offspring interactions selection. A distinction discuss som here. The p possible exp win’s writin special, soc and to argu and behavio 2. Darwin’ sexual sele Darwin ual selectio traits that survive in t advantage advantage t this distinc as Sexual S depends, no beings or to external conditions, but on a struggle between the individuals of one sex, generally the males, for the possession of er s porta ary s as d stat en na mple e cru may ut b ans i ent chie pre les, o fecte e Da envir effor r “rep ly th y, 19 te fu l and t res of fer d “cr ce fe le’s rypt d his d by rnal ale cr rkhe ecen d int with en n win’s on ca n su selec urph ual s sign the q p.98 ale c er to and v unde beca ity in are wini en t selec mpe (ferti e so(1859 [1872]) wrote two major books on evolution by he first, On the Origin of Species by means of Natural devoted primarily to evolution by natural selection, cond, The Descent of Man and Selection in relation to treats evolution under sexual selection. In 1860, while ork on the second book, Darwin wrote a letter to Asa efers in uncharacteristic dramatic language to traits planation in terms of natural selection, or the struggle ce: “I remember well the time when the thought of de me cold all over. . . now small trifling particulars of ten make me very uncomfortable. The sight of a feather k’s tail, whenever I gaze at it, makes me sick!” (from 2 [1958], p. 244). ock’s tail is part of a sexually selected communication se exaggerated complexity, like that of the human brain t al., 2005), is expected to characterize traits that are g social selection. The complexity of sexually selected tion is well illustrated in this issue. Social competition ultitude of sensory-response capacities, often more multaneously, as in the multimodal signals of golden- nakins (Barske et al, this issue) and spiders (Herberstein sue). Phonological and syntactical complexity is illus- engalese finches (see Suzuki et al., this issue); and Zuk this issue) discuss contributions that explore striking differences in brain and behavior. Here I briefly review properties of social selection and show why it can mplexity and exaggeration that exceeds that usually der natural selection. Understanding this distinction is or any neurobiologist or animal behaviorist interested tions of signal-response systems, for the properties of s depend on the context in which they have evolved. development of human infants, for example, shows a ern of slowness in aspects that reflect a prolonged phys- ence on others, while being precocious in aspects under tion for effective monitoring and manipulation of the n whom they depend (Hrdy, 2014). e of Neuroscience & Biobehavioral Reviews offers a t sexual selection and beyond. Clearly, there is more lution of the sexes than just sex as the production . But the evolutionary neurobiology of male–female requires clarity about what Darwin meant by sexual nd the meaning of sexual selection is elusive when the between natural and sexual selection is lost. So I briefly e prominent examples of sexual-selection amnesia oint is not to defend sexual selection theory as the best lanation for sexually dimorphic traits, or to regard Dar- gs as sacred text. The point is to show how easily the ial essence of sexual selection can disappear from view, e for its importance in understanding the neurobiology r of sexual interactions. s distinction between natural selection and ction insisted repeatedly on the distinction between sex- n and natural selection, with sexual selection favoring benefit their bearers “not from being better fitted to he struggle for existence, but from having gained an over other males, and from having transmitted this o their male offspring alone. It was the importance of tion which led me to designate this form of selection election” (1871 [1877], p. 210). “This form of selection t on a struggle for existence in relation to other organic the oth the im “ordin p. 209) The betwe an exa of mal We abo org opm the is to ma per Her social in the cess” o but on Murph ultima natura sequen terms tion an to indu ous ma Such c win an affecte or exte of a m (see Bi more r selecte Not betwe of Dar selecti tilizatio sexual (see M Sex threat about (1858, in fem togeth health Signals favored of qual signals 3. Dar Giv sexual cific co mates petitivex” (Darwin, 1859 [1872], p. 76). Darwin emphasized nce of the distinction repeatedly. He sometimes used election” to refer to natural selection (e.g. 1871 [1877], istinct from sexual selection. ement I find most helpful to clarify the distinction tural and sexual selection as social selection features – the prehensile organs (clasping antennae, and legs) staceans: suspect that it is because these animals are washed y the waves of the open sea, that they require these n order to propagate their kind, and if so, their devel- has been the result of ordinary or natural selection. . . if f service rendered to the male by his prehensile organs vent the escape of the female before the arrival of other r when assaulted by them, these organs will have been d through sexual selection (Darwin 1871 [1877] p. 209). rwin distinguishes between the non-social and the onments – a struggle with waves vs conspecific rivals t to hang onto a mate. Both can affect “mating suc- roductive success,” and both can occur simultaneously, e social struggle falls under sexual selection (see also 98). This passage also illustrates the difficulty, and the tility, of trying to make an absolute distinction between sexual selection in view of discoveries made in sub- earch. Sexual selection is now more broadly defined in tilization success, to include male-male sperm competi- yptic female choice,” or contests where a male competes males to process the male’s sperm, discard the previ- sperm, oviposit more quickly, resist further males, etc. ic social contests among rivals were invisible to Dar- contemporaries, and so were unsuspected even when visible morphology (such as elaborate male genitalia) behaviors, such as movements by the clasping organs ab that might affect the internal responses of a female ad and Møller, 1998; Eberhard, 1985, 1996, 2009). These tly studied phenomena expand the scope of sexually eractions envisioned by Darwin’s example. standing the difficulties of a consistent distinction atural and sexual selection, given the clear evidence intended meaning the Darwinian concept of sexual n be reworded as social competition for mates or fer- ccess via courtship and male-male contests (“Darwinian tion”) as contrasted with non-interactional definitions y, 1998). election often involves communication – courtship and als – but the signals need not convey any information uality of the sender under natural selection. Darwin ) recognized that health and vigor could play a role hoice, and that natural and sexual selection may act favor the same traits. But he consistently classified igor signals as products of natural, not sexual selection. r sexual and other kinds of social selection (see below) are use of their effects on others, not their value as indicators other contexts. It is for this reason that sexually selected sometimes considered “abstract” or “symbolic.” an sexual selection as social selection he many examples discussed by Darwin, Darwinian tion is a kind of social selection, or interactive intraspe- tition for resources, where the contested resource is lization success). Darwin recognized two kinds of com- cial behavior under the heading of sexual selection: M.J. West-Eberhard / Neuroscience and Biobehavioral Reviews 46 (2014) 501–508 503 courtship – contests of attractiveness, or ability to stimulate poten- tial mates in ways favorable to mating; and battle – contests of strength, w among riva sexual” and tially confu mates, whe Example and domina of queens i parental att Brock and H Kölliker, 20 1983, 1984 force the pa kind of non female ador Darwin kinds of soc orful traits under sexu females as sexual trans occur durin novelty (se did not focu reasons see there might tion”), on m (1871 [1877 females are a reversal o attributed t For a revie 2001; Bean social comp or displayin competitive Social (in Darwinian and both m insist on di sons for th whose pecu be explaine they evolve 4. Special p The soci special evo under natu Some of the on differen that are unu specific (We of sexual s tion). Speci (for more c West-Eberh 4.1. The un Social se in part bec unending races among rivals: the social environment for social selection changes with every improvement in a sexually com- e tra lutio wit doe ion b es o [187 ry or ions s mo rd to r, eit e lim as t on.” e po er (1 on to that t e con ishe ts in roce nce oluti e dis e run exag uant e in bine umb , the ffect size ngle x” [r Fish siven natu refer , foll cestr mod ly to that w ph er s of m uch on (e ction 984 e rel tions ial co sexu every l selehere the interactions involve weaponry and threats ls. Although sometimes courtship is called “inter- combat “intra-sexual” sexual selection, this is poten- sing: all sexual selection is intra-sexual competition for ther via courtship or battle (see also Fisher 1930, p. 147). s of non-sexual social competition include territorial nce (status) competition among females, worker choice n social insects, and competition among offspring for ention (see Amundson, 2000; Benenson, 2013; Clutton- uchard, 2013; Lyon and Mongomerie, 2012; Mas and 08; Stockley and Bro-Jorgenson, 2011; West-Eberhard, ). Monogamous females may have displays that rein- ir bond and increase paternal investment, an additional -sexual social selection (e.g. see Servedio et al., 2013 on nments in the great crested grebe). did not generalize beyond sexual selection to other ial selection. He thought that most exaggerated or col- of females in monomorphically bright species evolved al selection on males and then were transferred to a pleiotropic effect with no evolved function. Cross- fer in the expression of sexually selected traits does g evolution and is an important source of evolutionary e West-Eberhard, 2003, chapter 15). Although Darwin s on the competitive behavior of females (for possible Andersson, 1994; and Hrdy, 2013), he did suggest that be mutual sexual selection (“a double process of selec- ales to choose females and on females to choose males ], p. 225). Darwin also noted sex-role reversals, where the sexually selected sex, and associated them with f sex roles in parental investment, an insight usually o later authors like Bateman (1948) and Trivers (1972). w on male mate choice in insects, see Bonduriansky, i et al., this issue). But females engage in other kinds of etition, e.g. territorial or dominance interactions, using g male-like or female-limited bright or complex socially traits (see West-Eberhard, 1978, 1983, 1984). cluding sexual) selection and natural selection are both selection – differential fitness, or reproductive success, ay influence the evolution of a particular trait. So why stinguishing between them? There are powerful rea- e distinction in studies of sensory-response systems, liarities, exaggeration, and degree of complexity can d or even predicted by the selective context in which d. roperties of social selection al essence of sexual selection gives rise to a number of lutionary properties seldom or never shown by traits ral selection alone (see Wolf et al., 1999 for a model). se properties enhance the diversifying effect of selection t populations, promoting the evolution of phenotypes sually distinctive or extreme and population or species st-Eberhard, 1983); other aspects enhance the strength election (Rodriquez et al., 2013 discuss this distinc- al properties of social selection include the following omplete discussions see Lyon and Mongomerie, 2012; ard, 1979, 1983, 1984). ending nature of change lection promotes the evolution of extreme phenotypes ause combat and contests of attractiveness represent petitiv co-evo test is usually except parasit (1871 ordina condit tageou in rega anothe definit as long will go 4.2. Th Fish selecti noted nals ar fight (F Contes away p prefere the ev by som that th in trait each q increas So, com large n choice term e empha on a si parado The respon under such p (2008) the an (1981) “unlike dence any ne Und choice texts, s attenti or reje 1983, 1 4.3. Th genera Soc case of ual of naturait, so that there are moving targets and an unending nary race. Under natural selection, by contrast, the con- h a relatively unchanging environment, or one that s not change in response to progress achieved, a notable eing co-evolutionary races between species-specific r pathogens and their hosts. As expressed by Darwin 7], p. 226): “in regard to structures acquired through natural selection, there is in most cases, as long as the of life remain the same, a limit to the amount of advan- dification in relation to certain special purposes; but structures adapted to make one male victorious over her in fighting or in charming the female, there is no it to the amount of advantageous modification; so that he proper variations arise the work of sexual selection tential for runaway change under choice 930) extended Darwin’s interactional concept of sexual incorporate original insights based on genetics. Fisher he elaboration of traits involving combat or threat sig- strained to reflect “genuine prowess” or true ability to r 1930 [1958], p. 156; see also West-Eberhard, 1979). volving choice, by contrast, have the potential for a run- ss, with a genetic correlation between traits affecting and attractiveness producing mutual reinforcement of on of those traits until eventually slowed or checked advantage under natural selection (Fisher, 1930). Note, away process of ever-accelerating geometric increase geration applies not only to the quantitative increase in itatively variable stimulus and response, but also to the numbers of traits added – the complexity of displays. d with the relative lack of a ceiling for change, and the er and diversity of stimuli that can simultaneously affect runaway process has a greater potential to have a long- on sexual selection than argued by theoreticians who the limits to genetic variation under sexual selection quantitatively variable trait (sometimes called the “lek eview in Andersson, 1994]). erian runaway process begins with differential female ess (“preference”) to signals originally established ral selection, which is then exaggerated because any ence is favored by selection on preference itself. Price owing Fisher, emphasizes the “stimulatory value” of al naturally selected trait, and considers the Lande el of the process, which begins with spread due to drift, be of great importance” because there is so little evi- drift has been responsible for the origin and spread of enotypic trait (see also West-Eberhard, 2003, p. 144). ocial selection theory Fisher’s ideas regarding female ates can be extended to apply to choice in other con- as parental choice of offspring competing for parental .g. see Lyon et al., 1994), and worker choice (acceptance ) of competing queens in social insects (West-Eberhard, ). entlessness of social selection within and across mpetition within groups for access to resources – in the al selection, mates – affects every reproducing individ- generation in sexually reproducing species, whereas ction is not always so consistent: not every individual 504 M.J. West-Eberhard / Neuroscience and Biobehavioral Reviews 46 (2014) 501–508 of a population may be affected by a particular kind of predator, for example, or be subjected to the same range of climatic conditions. 4.4. The ver change in ne The ver ate change that modify see Trillo e signal com relationship diversificat ities of riva under selec stimulus–re getting or a on sensory receivers, du (4) imitatio ing; (5) indi (“good surv selection fo in combat tion of oth the tactics 1983). 4.5. The pot success Traits th narily stron with winnin lations whe where one o resource (e In gene terms of it competitive striking nat choice is b no direct in sexes invol than antago females. Th sexes are n investment 5. When to important I have v competent social comp the author( evolution o sometimes choice” in attention to appears in female cho view those tion (see be Sexual-s social aspec the symptoms and signs of sexual/social selection are recognized. A role for sexual or some other form of social selection should be gate e of me the ful m rphi of su omo der ed g ies- genc pop les; h in c bserv tship ously ual-s l an Dar en re on a ise h nes on, w r the ppen e an rtent ing y Fis ual s lack excep o w e, e verg on fo ned heno ts o s rec inter ed u May lana rd, 1 biolo as th ing of t ual s with ture nd o en im hen chesy large number of factors and cues that can initiate w directions (see West-Eberhard, 1983) y large number of factors and cues that can initi- in new directions include (1) environmental factors the effectiveness of signals and fighting tactics (e.g. t al., 2012 on the effect of bat predation in reducing plexity; Price (1998, 2008) extensively discusses the between social selection and ecological factors for ion in birds); (2) multiple pre-existing sensory capac- ls and courted individuals. Every sensory modality, tion in numerous evolutionary contexts, can produce sponse systems that can secondarily serve as attention- ttractive devices under social selection (see Ryan, 1990 exploitation); (3) variations in the responsiveness of e to such variables as age, condition, and experience; n of successful individuals in species capable of learn- cators of superior fitness favored under natural selection ival genes”), and subsequently modified under social r attractiveness per se; and (6) the advantage of novelty and display, where a new trait can arrest the atten- ers and thereby affect their preferences, or subvert of unprepared rivals (Darwin, 1871a; West-Eberhard, ential for very large differences in reproductive at influence sexual/social contests are under extraordi- g selection (large fitness differences can be associated g vs losing under social selection), especially in popu- re individuals are obliged to compete within groups r a few group members can monopolize access to some .g. leks, shared territories, or within shared nests). ral, selection on males and females is synergistic in s effects on sexually selected traits (i.e., the socially traits of males), and this helps account for the often ure of traits under sexual selection. Even when female ased on male victory in contests among males, with teraction or Fisherian genetic correlation between the ved, there is mutually reinforcing synergism rather nism, in the traits favored by selection on males and is synergism applies even when the interests of the two ot identical, due to underlying differences in parental . suspect that sexual/social selection may be ery often seen publications and lectures by otherwise and even eminent biologists, where sexual selection or etition ought to be considered but is not, even while s) labor mightily to give a thorough account for the f a trait. Innocent ignorance about sexual selection is betrayed by misuse of its concepts, like assuming “male a species whose polygamous mating system justifies female choice instead. And the term “sexual selection” titles of papers dedicated to subjects like good-genes ice and sexually antagonistic co-evolution, that in fact phenomena as dominated by natural, not sexual, selec- low). election amnesia and the related problem of neglect of ts of sexual selection are easily remedied problems once investi or mor • Extre tails, color dimo sion mon be un • Mark spec diver lated beet • Use by o cour obvi 6. Sex natura The has be ning so a conc tion am selecti tion fo that ha of mal inadve Dur biolog to sex plete b some me wh the tim ior. Di selecti concer gent p produc specie costly diverg 1937; an exp Eberha many nition a blink eration a role. Sex 1970s, the na 1972, a But th again w approad, though it is not proved, whenever a trait shows one the following symptoms: development or striking complexity (as in peacock’s horns of beetles, animal genitalia, the human brain, the ouths of nestling birds), sometimes leading to sexual sm or rank-dependent polymorphism in the expres- ch traits. When a striking or complex trait is sexually rphic, female-limited, or observed in immatures it may non-sexual social selection. eographic variation, phylogenetic diversification, or and population-specificity of a trait, suggesting rapid e of genetically isolated populations, or culturally iso- ulations capable of learning (plumage of birds; horns of uman languages and dialects). ontests or socially competitive displays as revealed ations of behavior, as in observations of combat or where colorful plumes or extreme morphologies come into play. election amnesia and the interplay between d sexual selection winian concept of sexual selection as social selection peatedly forgotten within evolutionary biology, begin- fter publication of Darwin’s treatise on the subject (for istory of reasons see Andersson, 1994). Sexual selec- ia also characterizes many modern discussions of sexual hich often emphasize the importance of natural selec- evolution of sexual signals and female choice. When s rich possibilities for insights regarding the evolution d female neurobiology, behavior, and morphology are ly lost from view. the mid-twentieth century synthesis in evolutionary her (1930) importantly extended Darwin’s approach election (see above), but there was a nearly com- out of the theory among organismal biologists (with tions, e.g. Huxley, 1938). This affected students like ere steeped in the organismic evolutionary biology of specially as applied to speciation and animal behav- ence between populations was seen as a result of r adaptation to ecological differences, and when it sexual behavior and associated morphology the diver- types were seen primarily or even exclusively as f selection for pre-mating reproductive isolation or ognition – traits evolved under selection to prevent breeding between incompatible gene pools that had nder natural selection (see especially Dobzhansky, r, 1963). Despite the weakness of this argument as tion of elaborate secondary sexual traits (see West- 983; Eberhard, 1985, 1996) it persists in the minds of gists today. So any casual mention of species recog- e explanation for such traits should be regarded as red arrow pointing toward a need for careful consid- he possibility that sexual selection could have played election theory seemed to undergo a revival in the early interest in its relationship to parental investment and of mating systems (Emlen and Oring, 1977; Trivers, ther authors, including Mayr, 1972, in Campbell, 1972). portant components of Darwin’s idea were forgotten vast areas of research on sexual behavior focused on that propose alternative explanations (next section). M.J. West-Eberhard / Neuroscience and Biobehavioral Reviews 46 (2014) 501–508 505 6.1. Natural and sexual selection in signal evolution One rem of sexual sig Males explo competitive probably us and then co tion for fer reach unus that would Eberhard, 2 the effects selection ca traits (Price or complem critical reso properties o systems to l ral selection and social/s 6.2. “Good- by socially-s “Good ge are indicato is easy to fo choice as an addition, to elaboration natural sele good attrac choosy fem sexual/socia genes, e.g. good compe Sexually ness per se – Thus, the he effective as tures other social statu be enlarged that make rival. These with the ab red. While of value und embellishm which in tu Numero resistance strength an 1982; Ham facial patch this Issue) an incident to disease selected, in females. Ind males that parasites (s Extreme the evolutio sexual selec morphology are described as “sanimetric” (p. 794) with males usu- ally the “sanimeter” or “health index” sex (p. 798)). Although this ic” ( duce (e.g. on, 2 r se. ale c cond tition etry ): (1) (diff es) se icato l sele s (ag pote for g t hon exity a to ion o grea ve b tc.) a lity, or va icato stem e hea n th s infli ndica d no n for d in pend less mero mpo s in b ents rturn elate call t good ds o toric selec lectio nflic ther s con s stri to th we, incre to co lving neg selec ors c y synedy for sexual selection amnesia is to see the evolution nals as interplay between natural and sexual selection. it a great variety of neuro-hormonal channels during and manipulative sexual interactions. Those channels ually, perhaps always, originate under natural selection, me under sexual selection during interactive competi- tilization success. Then sensory-response systems can ual levels of elaboration, plasticity, and diversification not occur under natural selection alone (see West- 003; Price, 2006). Natural selection may ultimately curb of sexual selection, and good condition under natural n help bear the costs of exaggerated socially selected , 2006). But social interactions can take precedence over ent survival selection when they determine access to urces like mates and other resources; and the special f socially mediated selection can drive neuro-hormonal evels of elaboration beyond those achieved under natu- alone. These features of the interplay between natural exual selection are often forgotten. genes” indicators and the corruption of honest signals elected noise nes” interpretations of sexual signals argue that signals rs of genetic quality under natural (survival) selection. It rget that once a phenotypic trait is favored under female indicator of genetic quality it is inevitably subject, in sexual selection for enhanced signal quality, and its as an effective signal comes under sexual selection, not just ction (indicator function) (Fisher 1930), which favors tiveness genes alongside good survival genes. Then ales produce “sexy sons” as well as healthy sons. Under l selection “good genes” means good social-interaction genes that contribute to being a good stimulator, or a titive fighter or manipulator of conspecifics. selected elaborations, then, enhance signal effective- they are tools of success in sexual/social competition. alth-indicating red color of a feather may be made more a signal – and less effective as an indicator – by fea- than red color that enable an individual to improve its s, and thereby its access to resources. A feather may relative to normal feathers, adorned by added details it more conspicuous, or waved before a female or a embellishments and exaggerations have nothing to do ility to produce the color itself – the indicator value of energetic waving behavior may indicate further traits er natural selection, the attention-getting value of the ents are due to effects on success in social interactions, rn affect access to resources (in this case, mates). us traits preferred during mate choice correlate with to parasites and disease, or demonstrate physical d prowess (for many examples see Hamilton and Zuk, ilton, 2001). Thus, a signal like the diet-dependent red es of some male jumping spiders (see Herberstein in or the red color of a feather may have originated as al (unselected) byproduct of constitutional resistance or ability to sequester essential nutrients, and been addition, under sexual selection for attractiveness to eed, some ornaments can be produced only by those carry the genes for resistance against pathogens and ee Milinsky, this issue). advocacy of the good-genes approach, however, takes n of signals completely out of the realm of Darwinian tion (e.g. see Hamilton, 2001, where sexual displays and “eugen has pro health Hamilt tion pe Fem is a se compe asymm sperm choice ferenc on ind natura benefit The ground corrup compl This is evolut for the that ha vigor, e variabi indicat the ind tion sy into th betwee noise i as an i affecte weapo affecte will de A horn ing nu be as i Succes oppon or ove to be r To as in “ hundre in a his sexual ural se 6.3. Co Ano tions a female costly and Ro males tance as evo female sexual behavi therebHamilton and Zuk, 1982) approach to sexual selection d exciting discoveries linking sexual display to signs of Hamilton and Zuk, 1982 and others; partial review in 001), it has also led to amnesia regarding social selec- hoice based on strength and vigor (good survival genes) -order consequence of sexual selection via courtship among males, which originates due to the investment between the sexes (beginning with gametes, eggs and contests of male attractiveness (courtship) and female erential female responsiveness based on courtship dif- ts the stage for (2) the evolution of female choice based rs of male quality – genes beneficial to offspring under ction; or, in species with male parental care, offspring ain, under natural selection) provided by good fathers. ntial for social selection is always present as the back- ood-genes indicator selection and it can be expected to est signals with socially selected “noise,” increasing the of signals while undermining their value as indicators., pic of importance for neurobiologists interested in the f complexity: Indicators of health seem unlikely to account t complexity of sexual communication. The indicators een proposed (particular colors, brightness, strength or re quantitatively variable traits whose health-correlated not complexity, makes them useful indicators. Their lue depends on the strength of the correlation between r trait and the genes that affect health. But sexual selec- atically undermines that correlation, introducing “noise” lth-correlated signal as it builds, instead, a correlation e trait and its attractiveness to females. The same sort of cted by sexual selection on the value of combat strength tor of health and vigor, for successful male combat is t only by health and vigor but also by the efficacy of m, fighting behavior, and aggressive display, all features turn by social sexual selection. “In many cases, victory not on general vigor, but on having special weapons. . . stag or spurless cock would have a poor chance of leav- us offspring” (Origin, p. 69). And “. . . the shield may rtant for victory, as the sword or spear” (Origin, p. 69). attle depends not on health alone, but on the tactics of – whether they use weapons to push, pry, strike, pinch, rivals (e.g. see Eberhard, 1980) – variables not known d to health. he good-survival-genes hypothesis “sexual selection,” -genes sexual selection” (a search term that recovers f publications on Google Scholar) is an ironic twist seen al context because Darwin so strongly emphasized that tion covers phenomena not explainable in terms of nat- n. t theory, and sexually antagonistic co-evolution productive area of research views courtship interac- flict between the sexes – a battle of the sexes – in which ve to resist persistent male sexual interactions that are em in terms of natural selection (Parker, 1979; Arnqvist 2005). This results in “antagonistic co-evolution” as ase forcefulness to overcome increased female resis- stly interactions. Female responses to males are seen due to natural selection which favors self-protective ativity, not the positive female choice of Darwinian tion, where seemingly resistant female structures and an in fact screen for the mating acumen of males and ergistically select for its improvement during evolution. 506 M.J. West-Eberhard / Neuroscience and Biobehavioral Reviews 46 (2014) 501–508 Sexual selection with female choice also predicts male–female conflict – a point sometimes forgotten in discussions of sexual con- flict based o “narrow sen between th ference is im conflict the response sy selected con to the spec already des posed that should be s tionary neu two kinds o ary dynami impetus tha tion. So it is between th because the males of Po nistic confli attractivene Unfortun ory offer li based on n seminal pa some detai sons which In the mod the analyses sowed the s (but see Pa sively). The 2005) first 3) as akin t vigor, and a on misread (in the cited cannot be a of conflict t spread and mating or f more mani here of the choice invo and success is seen as clear negat fact that th resistance o italics mine ignores the “honesty”). Whethe conflict the under natur ity due to be on whether selected cos on a case-b of both inte Brennan an 1999; Parke ing activity is not enou 6.4. A conflict-theory paradox and the emergence of sexually synergistic co-evolution rea sug o its nefit- selec alue mpor with t the peci kins ction e in o rodu tives mati recog ersi ales not s sho male nce t agi ry ti the ired ait, ra imul l sele red t the the lutio drivi on – ive m fema o the at d hip s or? W e at accu aint goni are on (d e sig ntago or o s imp pre d nar erfow but a nce ina uniti ion a y Bre ion p n ann naturally selected conflict theory, therefore termed se” conflict by Brennan and Prum (2012). The difference e two kinds of conflict is not always clear. But the dif- portant especially for neurobiologists: narrow-sense ory sees the male–female co-evolution of sensory- stems as mutually antagonistic, whereas under sexually flict male–female co-evolution is synergistic, giving rise ial mutually reinforcing properties of social selection cribed (above). Some authors have unfortunately pro- attraction-preference and persistence-resistance conflict ynonymized, but this is profoundly mistaken for evolu- robiology, as shown by Brennan and Prum (2012). The f conflict are expected to have very different evolution- cs, with narrow sense conflict lacking the synergistic t is a special property of interactions under sexual selec- important, in a neurobiological context, to distinguish ese two interpretations of conflict, and not assume that re is an appearance of conflict, as in the “marathoner” listes leks (see Beani, this issue), narrow-sense antago- ct theory (force and resistance, rather than synergistic ss and choice) applies. ately the key references on narrow-sense conflict the- ttle guidance on how to distinguish between conflict atural vs sexual selection. Parker (1979, p. 130), in a per on sexual conflict theory states: “I have looked in l at the possible benefits which accrue to females via inherit the sexual selection advantages of their fathers. els which will follow, this effect will be omitted to keep simple” (emphasis not in the original). With that, Parker eeds for sexual-selection amnesia within conflict theory rker, 2006, where the topic is taken up more exten- major book on conflict theory (Arnqvist and Rowe, mischaracterizes Darwin’s view of female choice (p. o good-genes sexual selection, based on strength and s most common under monogamy, a conclusion based ing a passage from Darwin with the opposite intent passage Darwin was explaining why sexual selection s effective under monogamy). Under their description heory (p. 35) “male traits that decrease female fitness are exaggerated because females ‘prefer’ them (i.e., bias ertilization success toward males with exaggerated or pulative traits).” But there is little or no consideration sexually selected alternative, where positive female lves sensitive screening for males that are attractive ful manipulators of female responses. Positive choice overcome by female negativity (“resistance”) with a ive result for the evolution of sensory abilities: “The ese traits are costly to females leads to selection for r the evolution of insensitivity to them” (ibid, p. 35, ; see also Krakauer and Johnstone, 1995, which also possibility of signal value as stimulation not requiring r female resistance is better explained by narrow-sense ory (female negativity due to signal detriments to fitness al selection) or sexual selection theory (female selectiv- nefits to offspring of superior signaling genes) depends the sexually selected benefits overcome the naturally ts of the male trait to females. This can only be evaluated y-case basis using data that compare the expectations rpretations (as in Arnqvist and Rowe, 2005, pp. 40–43; d Prum, 2012; Eberhard, 2004a,b; Holland and Rice, r, 2006). Demonstrating only a cost to females of mat- , or a benefit for male signal behavior and morphology, gh. The theory leads t the be sexual ative v more i solidly conflic some s and Ad ral sele to mat ally rep alterna favors As most p tent m should female aging resista the dam lutiona reduce – requ that tr cost st natura its own conflic toward co-evo nistic, directi attract where tance t Wh courts behavi that ar should mote m of anta nature selecti of mal over a behavi than a The marke of wat occur, resista predom opport format cited b talizat Brennasoning behind narrow sense female-negative conflict gests a “conflict paradox” where antagonistic conflict own decline. Suppose that a male signal fails to pass cost threshold in the female required for spread under tion – the trait is so detrimental to females that its neg- under natural selection determines its evolutionary fate tantly than its value (to offspring) as a signal, and it falls in the framework of narrow-sense female-resistance ory. This is the case for aspects of forced copulation in es of waterfowl during the breeding season (Brennan -Regan, this issue). Still, there is a tradeoff under natu- on females between effective resistance and the need rder to reproduce: a perfectly resistant female in a sexu- cing species would not mate at all (see Parker, 1979 for to sexual reproduction that might result). If selection ng, how could selection not favor selective mating? nized by Arnqvist and Rowe (2005) mating with the stent male is selective mating. But the most persis- are also the most female-damaging males and they , under natural selection on females, be the winners: uld prefer (be selected to mate with) the least dam- s among the persistant ones, or they should evolve o the damage inflicted by those males. In either case, ng effects of persistence should be diminished over evo- me. Natural selection, then, should constantly work to importance of the condition – damage or cost females for the relevance of conflict theory to the evolution of ising the relative importance of sexual selection (low- ation of females). Paradoxically, then, conflict due to ction on females should promote conditions that favor uced importance over time: under the assumptions of ory natural selection should continuously move traits realm of sexual selection. Under sexual selection the n of males and females is synergistic rather than antago- ng sexual interactions in the same mutually reinforced toward increasingly effective weapons or threats, and ale traits, and away from harmful sexual interactions les “choose” persistant males only because their resis- m is imperfect. oes this mean for analyses of the stimulus–response ystems observed by students of neurobiology and ith or without conflict, stimulatory courtship devices the same time attractive and low in cost to females mulate during evolution more than do traits that pro- enance of costly conflict. The paradoxical self-limitation stic conflict means that courtship devices observed in likely to evolve toward increasing influence of sexual ifferential attractiveness) as selection lowers the costs nals. When synergistic sexual selection predominates nistic interactions (e.g. see Huber, 1995) the choosy f females is better described as selective cooperation erfect resistance to male persistence. dicted occurrence of positive selective mating despite row-sense conflict may be exemplified in some lineages l, where both narrow-sense conflict and courtship re in temporally separate compartments. Persistence- conflict marked by frequent forced copulation tes during Spring breeding, whereas courtship affording es for female choice takes place during Winter pair nd has the greater effect on male fitness (Davis 2002, nnan and Adkins-Regan, this issue). This compartmen- rotects choice from interference by forced copulations. d Prum (2012) discuss vaginal pouches and other M.J. West-Eberhard / Neuroscience and Biobehavioral Reviews 46 (2014) 501–508 507 features of the female reproductive tract that may have evolved as cryptic anatomical mechanism of choice in response to forced extra-pair males to de age” (Brenn to reassert t 6.5. Post-co female choic The term tial to focu socially sel 2001 on thi petition em sperm com that permit (see Eberha ual selectio nature of m synergistic female-influ set aside, an In keepi sperm com phology sub species spe primarily in under natur of male mo selection. 6.6. Sensory origins of so Courtshi ago realized existing res become a “s a particular 11). Ryan (1 of pre-exist (Ryan, 1985 also Enquis for neural n ary interact that he calls The assi of naturally the origin o selected eff signal subje sexual selec acteristics co-evolutio tion of pre- ability to ev could jump choice unde not with ce their origin The imp selected mo except when the female r of contexts males (West-Eberhard, 1979). Examples of sensory traps that are exploited by males are the urgent response of a mother monkey to nt’s or-es resp ction clus biolo er s s in mpe This ion, bora ceed cial i rent oduc ion le orph um, oluti on. S or ba hen nce c ation tuall on r er, f used eque ous y co eview y is nd fo elec r, tec l and beha d. St ction havi ribut f con on to a vis on. wled critic erha Price veryt nces en, T., 155. on, M. , G., R , A.J., copulations, for these mechanisms “force unwanted posit their sperm further from the sites of sperm stor- an and Adkins-Regan, this issue) and “allow females. . . heir choice” (Brennan and Prum, 2012, p. 2335). pulatory sexual selection: sperm competition or e? , and the concept, of sperm competition has the poten- s so strongly on male-male gamete interactions that ected female choice may be forgotten (see Simmons, s and other aspects of sperm competition). Sperm com- phasizes male-male combat at the gametic level. But pete within females, on a female-defined playing field s what has been called cryptic (internal) female choice rd, 1985, 1996). When the female-choice aspects of sex- n are forgotten in this brand of partial amnesia about the ale-male competition, then the possibility of a sexually co-evolutionary race affecting sperm structure and the encing traits associated with gametic competition is d assumed to be unimportant. ng with the importance of cryptic female choice and petition, male genitalia, like other kinds of male mor- ject to sexual selection, are often highly complex and cific; and it is usually difficult to argue that they are struments of male-male combat, or primarily evolving al selection. Indeed, male genitalia may be the aspects rphology most likely to be pure products of sexual exploitation and sensory traps: natural-selection cial signals. p signals are a kind of communication. Ethologists long that communication systems in animals start with pre- ponses that permit a particular movement or cue to ignal” – an input produced by one individual that evokes response by another (review in Smith, 1977, chapter 990) has emphasized the role of sensory-exploitation ing female responses, beginning with his classic studies ) of sexual selection and communication in frogs (see t and Arak, 1993, 1998; Ghirlanda and Enquist, 1998 etwork models; Endler, 1992 on complex evolution- ions between sensory systems, signals and environment “sensory drive”). gnment of a female response to sensory exploitation selected responses alone is eminently reasonable for f a particular male signal, and for certain naturally ects on subsequent evolution (Endler, 1992). But any ct to choice is potentially subject to modification under tion. Then a correspondence between male signal char- and female sensory capacities could be a product of n under sexual selection rather than sensory exploita- existing capacities due to natural selection. The built-in aluate stimulus intensity of naturally selected stimuli -start the accelerated evolution of attractiveness and r sexual selection. So the nature of derived signals can- rtainty be attributed to sensory exploitation except at . ortance of sensory exploitation independent of sexually dification is likely limited to the origin of new signals the response is due to a sensory trap – a situation where esponse is so strong and unhesitating in a wide variety that it is permanently subject to sensory exploitation by an infa predat 2003), to sele 7. Con neuro Und succes cific co mates. evolut the ela not ex tive so as diffe can pr evolut and m In s the ev selecti threat even w resista exploit Mu selecti (consid fishes high-fr enorm sociall brief r synerg back a social s vs wa natura neuro- justifie of sele and be more t kinds o selecti to sex, selecti Ackno For sica Eb Trevor with e Refere Amunds 149– Anderss Arnqvist Batemancry of distress (Moynihan, 1970); and the emergency cape response of female fiddler crabs (Christy et al., onses so crucial that they may be relatively immune for modification in the context of sexual selection. ion: natural and sexual selection as causes of gical evolution exual/social competition there is an unending race for social environments, where interaction with conspe- titors screens off access to critical resources such as implies a new set of expectations for neural system with indicator-honesty not required and no limit to tion of signal-response complexity as long as costs do resource-accrual benefits of social success. Competi- nteractions, especially those that involve choice (such ial responsiveness to signal variants during courtship), e a self-accelerating process of sexually synergistic co- ading to extreme complexity in the neural, behavioral, ological traits that affect social selection. natural selection is a relatively conservative force in on of sensory-response systems compared to social o extreme elaboration of male traits used in courtship, ttle indicates that sexual selection is likely important, natural selection (good survival genes, persistence- onflict, sexually antagonistic co-evolution, or sensory ) is involved. y reinforcing synergism between natural and sexual esults in some of the most extreme traits known or example, the powerful electric discharge of electric in both signaling and predation (Stoddard, 1999); ncy sound in bats (see Kingston et al., 2001); and the size of dinosaurs – all traits with both trophic and mpetitive functions; see West-Eberhard, 2003 for a ). A spectacular product of natural-social selection the human brain, whose analysis has led researchers rth over the conceptual border between natural and tion, between tool-making vs spear-throwing, foraging hnical vs Machiavellian and empathetic skills. Both social selection are likely involved in the evolution of vioral complexity, and an either-or explanation is not ill, it is important to distinguish between the two kinds , especially in research on complex neuro-endocrine oral systems involved in social interactions. It is one e to Darwin’s genius that he seemed to anticipate the troversies discussed here when he saw beyond natural write about The descent of man and selection in relation ion of human evolution that features social aspects of gements al suggestions and discussion I thank John Christy, Jes- rd, William Eberhard, Kyle Harms, Ximena Miranda, , Rafael Rodriquez and the editors. Not everyone agreed hing but even that helped. 2000. Why are female birds ornamented? 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