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1160 Animal Signals and the Overlooked Costs Of Evolution, 59(5), 2005, pp. 1160±1161 ANIMAL SIGNALS AND THE OVERLOOKED COSTS OF EFFICACY1 MICHAEL J. RYAN2 AND MOLLY E. CUMMINGS Section of Integrative Biology C0930, University of Texas, Austin, Texas 78712 2E-mail: [email protected] Received March 22, 2005. costly; handicaps can make it more costly, but lack of hand- The most striking aspects of many animals are signals. icap does not make it cost free. This book concentrates on Thus one might expect Animal Signals by John Maynard strategic costs, but offers some tantalizing discussions of ef- Smith and David Harper to discuss the detailed biology of ®cacy costs, which the authors suggest are underappreciated. this half of the communication dyad. Not so. Instead, they We second that notion but feel it is not strong enough. concentrate on a single question, why signals are reliable, The most basic ef®cacy costs of signaling are incurred in and emphasize one methodology to its solution: game theory. creating its morphology, behavior, and neural circuitry. In ad- Although not embracing the entire biology of signaling, the book grapples with a continuing problem. dition, some animals scour the environment to obtain their Signals evolved to communicate information and manip- signals; bowerbirds steal decorations for their bowers (Borgia ulate receivers to the signaler's bene®t. Similarly, the re- and Mueller 1992), and some moths sequester plant alkaloids ceiver's response to signals is under selection to promote its for the ¯occulent showers they bestow upon females (Conner ®tness. The issue at hand is the con¯ict between signal and et al. 2000). There are also costs imposed by the environment. receiver: what keeps the signaler from providing false in- Once the signal is built, it then needs to be presented against formation to the receiver? an acoustically noisy and visually cluttered world. When back- Zahavi (1975) explained signal reliability with the hand- ground noise is loud, ®nches increase their songs' amplitude icap principle: males evolve costly signals to indicate their to be heard above the ambient din (p. 16). More generally, underlying genetic quality for survivorship. The authors de- the evolution of signals for environmental contrast is well tail how this theory was rejected enthusiastically by modelers, known (e.g., Morton 1975). In his sensory drive model, Endler including Maynard Smith (1976; see also Kirkpatrick 1986), (1992) argues that factors such as ambient light, background and resurrected as enthusiastically a decade later (Pomian- pattern, and the sensory capabilities of predators can all be kowski 1987; Grafen 1990). important factors in signal evolution. Signal ampli®ers or ex- Maynard Smith and Harper, however, argue convincingly aggerators, we are told (p. 47), might be viewed similarly. that although suf®cient, the handicap principle is hardly nec- Substantial features of signals result from selection for envi- essary to explain reliable signals because not all signals are ronmental contrast, and thus are driven by ef®cacy costs. costly, and not all costs are handicaps. Several situations Ef®cacy costs are incurred in achieving two other types of enforce signal reliability without handicaps: signalers and contrast, which we call social and neural contrast. To transmit receivers share common interests, both parties have con¯ict- a signal reliably, it must also contrast against the social en- ing interests yet agree on preferences for outcomes, cheaters vironment. One who can produce a different syllable or color, are punished, or signals cannot be faked. In this last and most or present a signal out of phase with the cacophony of one's interesting case, signals are constrained to be reliable by competitors, might gain social contrast, making its signal morphology and physiologyÐthis type of signal is an index more noticeable and thus salient to the receiver. At the level (p. 60; see also Enquist 1985). The authors offer as an ex- of the individual, receivers can habituate to signals. Complex ample the frequency of a red deer's call being constrained bird song, for example, might have evolved for ``neural con- by larynx size. Males can evolve larger larynges and behav- trast,'' to release receivers from habituation at the behavioral, iors to expand its size, but once such innovations are ®xed neural, and gene expression levels (reviewed in Ryan 1998b). in the population, call frequency again becomes a reliable These varied ef®cacy costs of contrast could initiate an arms index (p. 46). race that culminates in the extreme elaboration of signals Many signals that are not indices are costly to the signaler. associated with, though indistinguishable from, Fisher's run- Is this cost prima facie evidence for a handicap, as Zahavi away sexual selection. might suggest? No. ``Demonstrating that a signal is costly, The most intriguing example of an ef®cacy cost given by therefore, is not evidence that it is a handicap.'' (p. 16; see the authors is the behavior involved in presenting the signal. also Ryan 1998a) Why? The authors point out that there is A nightingale spends most of the night calling and can lose more to signaling than reliability, and they identify a di- 5±10% of its body weight while doing so (p. 16). This seems chotomy of signal costs. Ef®cacy costs are those required to the perfect candidate for a handicap: males courting vigor- ensure that signals can be transmitted ef®ciently to the re- ously to display their overall genetic health to females. But ceiver (p. 73). Strategic costs are additional costs that ensure suppose males need to attract females ¯ying overhead and signal reliabilityÐZahavi's handicaps. Effective signaling is unseen; then continuous display is the only option. Thus, when females are unpredictable in space or time, vigorous 1 Animal Signals, by John Maynard Smith and David Harper. and constant display is an ef®cacy cost and not an index. We Oxford University Press, Oxford, U.K. 2003. ix 1 166 pp. HB expect this to be so for most long-distance signaling. Many $114.50, ISBN 0-19-852684-9; PB $44.50, ISBN 0-19-852685-7. animals invest considerably in time, energy, and predation 1160 q 2005 The Society for the Study of Evolution. All rights reserved. BOOK REVIEWS 1161 risk to casting sounds, odors, and re¯ected light upon the ni®cance of the data. It has made critical contributions to environment with no assurance that anyone is listening, signal evolution, but, as the authors themselves insinuate, it smelling, or watching. Although often viewed as handicaps, is time to move on to a more integrative biology of animal perhaps these investments are ef®cacy and not strategic costs. communication. The discrimination will not always be clear. For instance, the This book is typical of several previous books by Maynard authors suggest that courtship vigor in fruit ¯ies (Maynard Smith, such as those on sex (1978) and game theory (1982): Smith 1956) is an index of overall male health and thus a it is engaging, short, to the point, and emphasizes arguments reliable indicator of male genetic quality to females (pp. 51± from ®rst principles rather than exhaustive documentation. 52). Although possible, vigorous signaling might only in- Anything that Maynard Smith says is worthy of our undivided dicate that the male is a good signaler. A frog's metabolic attention, and this volume co-authored with Harper is no ex- rate increases manifold when he calls, thus the notion that ception. Sadly, this is our last opportunity to have our attention the male is advertising his physical ®tness does not seem engaged by a new work from this incredible intellect, as John, farfetched (see e.g. Welch et al. 1998). But Taigen and Wells a dear friend, passed away as we ®nished chapter 2. (1984) found no relationship between calling effort and total aerobic capacity in American toads. Are female toads being LITERATURE CITED fooled by cheating males, or are we the ones being fooled Bradbury, J., and S. L. Vehrencamp. 2000. Economic models of by assigning the wrong function to signaling? animal communication. Anim. Behav. 59:259±268. Of the many lasting contributions of John Maynard Smith, Borgia, G., and U. Mueller. 1992. Bower destruction, decoration the use of game theory to model animal behavior is most stealing and female choice in the spotted bowerbird Chlamydera maculata. Emu 92:11±18. prominent (e.g., Bradbury and Vehrencamp 2000). The au- Conner, W. E., R. Boada, F. C. Schroeder, A. Gonzalez, J. Mein- thors have used these models like a surgeon's tool to dissect wald, and T. Eisner. 2000. Chemical defense: bestowal of a the assumptions and consequences of the handicap principle nuptial alkaloidal garment by a male moth on its mate. Proc. in general, and reliable signals in particular. The conclusion, Natl. Acad. Sci. USA 97:14406±14411. Endler, J. A. 1992. Signals, signal conditions, and the direction of as we note above, is that the handicap principle is one, but evolution. Am. Nat. 139:S125±S153. only one, of several scenarios that can achieve reliable sig- Enquist, M. 1985. Communication during aggressive interactions nals. But the authors also note that game theory is not an with particular reference to variation in choice of behaviour. ideal approach for analyzing communication systems in- Anim. Behav. 33:1152±1161. volved in sexual selection in which there cannot be a single Enquist, M., and A. Arak. 1998. Neural representation and the evo- lution of signal form. Pp. 21±87 in R. Dukas, ed. Cognitive optimum (p. 12). Where simple economic models fall short ethology. Univ. of Chicago Press, Chicago. in addressing the important factors in sexual signaling evo- Enquist, M., A. Arak, S. Ghirlanda, and C.-A.
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