Dispatch R523 prototype is significantly larger than the brain flexibly shifts the reference 9. Leopold, D.A., Bondar, I.V., and Giese, M.A. (2006). Norm-based face encoding by single the one based on voice adaptation. point as we become familiar with neurons in the monkey inferotemporal cortex. Moreover, this relationship was other people’s voices. Also, what is Nature 442, 572–575. stronger than the relationship between the fidelity with which prototypes 10. Andics, A., McQueen, J.M., Petersson, K.M., Gal, V., Rudas, G., and Vidnyanszky, Z. (2010). TVA response and the distance to the represent certain features, and which Neural mechanisms for voice recognition. androgynous prototype. These features, or life experiences, have a Neuroimage 52, 1528–1540. 11. Bruckert, L., Bestelmeyer, P., Latinus, M., additional results strengthen the case greater influence on the formation of Rouger, J., Charest, I., Rousselet, G.A., for the norm-based coding of voice prototypes? Kawahara, H., and Belin, P. (2010). Vocal identity in the TVA. No doubt, studying these issues will attractiveness increases by averaging. Curr. Biol. 20, 116–120. Nonetheless, it is unlikely that continue to provide insights into how 12. Kanwisher, N., McDermott, J., and Chun, M.M. norm-based coding and we so effortlessly identity others and (1997). The fusiform face area: a module in human extrastriate cortex specialized exemplar-based coding accounts are how this process comes to a grinding for face perception. J. Neurosci. 17, mutually exclusive. For instance, halt for people with face or voice 4302–4311. exemplar-based coding might recognition deficits. We will possibly 13. Kayaert, G., Biederman, I., Op de Beeck, H.P., and Vogels, R. (2005). Tuning for shape predominate in certain brain regions, or also better understand how judges like dimensions in macaque inferior temporal when a prototype has not been formed Simon Cowell evaluate exceptional cortex. Eur. J. Neurosci. 22, 212–224. or is difficult to form. Also if many voices/faces, in relation to those that 14. Rhodes, G., Jeffery, L., Boeing, A., and ‘prototypes’ exist, norm-based coding we as a society might not find as Calder, A.J. (2013). Visual coding of human is difficult to distinguish from mesmerizing as the neurons in our bodies: Perceptual aftereffects reveal norm-based, opponent coding of body identity. exemplar-based coding. brains. J. Exp. Psychol. Hum. Percept. Perform 39, 313–317. Glimpse ahead and the ‘Mysterious’ References 15. Nosofsky, R.M. (1992). Exemplar-based 1. Latinus, M., McAleer, P., Bestelmeyer, P.E.G., approach to relating categorization, Prototype and Belin, P. (2013). Norm-based coding of identification, and recognition. In A psychological curiosity is that the voice identity in human auditory cortex. Curr. Multidimensional Models of Perception and Cognition, F.G. Ashby, ed. (Hillsdale, NJ: brain apparently can form a prototype Biol. 23, 1075–1080. 2. Belin, P., Zatorre, R.J., Lafaille, P., Ahad, P., Erlbaum), pp. 363–393. without ever experiencing it. In a and Pike, B. (2000). Voice-selective 16. Palmeri, T.J., and Gauthier, I. (2004). Visual classic study, Posner and Keele [19] areas in human auditory cortex. Nature 403, object understanding. Nat. Rev. Neurosci. 5, 309–312. 291–303. presented participants with many dot 3. Perrodin, C., Kayser, C., Logothetis, N.K., and 17. Grill-Spector, K., and Malach, R. (2001). patterns, which were synthesized by Petkov, C.I. (2011). Voice cells in the primate fMR-adaptation: a tool for studying the functional properties of human cortical distorting a prototype pattern. temporal lobe. Curr. Biol. 21, 1408–1415. 4. Quiroga, R.Q., Fried, I., and Koch, C. (2013). neurons. Acta. Psychol. 107, Although participants never saw the Brain cells for grandmother. Sci. Am. 308, 293–321. prototype during an exposure phase, 30–35. 18. Kahn, D.A., and Aguirre, G.K. (2012). 5. 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Genital Evolution: Cock-a- Biology, we get an answer to the Doodle-Don’t second question in a paper by Herrera et al. [4] that describes a developmental mechanism Losing the penis in species with internal fertilization may seem paradoxical, responsible for the loss of intromittent but birds have managed to do it multiple times. A new study addresses one function in the avian penis. developmental mechanism responsible for penis reduction in birds, and opens Only three percent of avian species the door to further examination of this little understood evolutionary belonging to two main clades have phenomenon. retained the ancestral copulatory organ: the Paleognathes (e.g., Patricia L.R. Brennan the loss of an organ that seems crucial ostriches, kiwis and tinamous), and the to internal fertilization, and how exactly Galloanseridae (e.g., chickens, turkeys, Most amniotes with internal fertilization can a penis be lost? The answer to the megapodes, cracids and ducks) [1]. All have a penis, with the exception of first question is still largely unresolved other birds have completely lost the most birds [1]. What could have driven [2,3]. However, in this issue of Current penis. Avian penis evolution is complex Current Biology Vol 23 No 12 R524

elegantly demonstrating that Bmp4 expression is both necessary and sufficient to regress growth of the penis. Bmps are involved in the development of several other organs [12], so their role in genital reduction suggests the possibility that the loss of the intromittent function of the avian penis may have resulted from pleiotropic selection on another organ system, rather than selection for Figure 1. Avian penis diversity. reduced genitalia per se. If true, Avian penises can be intromittent (A; Rhynchotus, a tinamou), non-intromittent (B; Crypturel- this could explain the seemingly lus), or completely absent (C; Leipoa). paradoxical loss and regression of genitalia in birds. However, the five (see Figure 1Ain[4]). In addition to the regulation of genital growth and independent evolutionary reductions loss of the penis in the ancestor of patterning that are already known and losses of intromittent penis all Neoaves, birds have experienced in mammals would explain the function have occurred in avian multiple reductions of the penis’ differences in morphology of the groups that differ greatly in ecology, intromittent function (at least once in avian penis. morphology and behavior. While most tinamous and twice in galliformes) One possible developmental route tinamous have an intromittent penis and another complete penis loss (in a for the chicken penis to become (Figure 1A), those in the genus megapode) [5]. Herrera et al. provide a non-intromittent would be for it to Crypturellus have a non-intromittent developmental picture of how birds can simply stop growing. Expression of Shh one that is very different from the transition from a fully intromittent to a (a morphogenic protein) and Hoxa13 non-intromittent chicken penis non-intromittent penis by examining and Hoxd13 (transcription factors), is (Figure 1B) [5]. Crypturellus are small genital development of chicken and known to be involved in promoting ground-dwelling forest birds with duck embryos. The chicken penis is genital growth in mammals [9,10]; exclusive male incubation and parental non-intromittent; and although it swells however, their expression was no care, and mating systems ranging during copulation and may help to different between chicken and duck. In from monogamy to promiscuity [13]. direct the ejaculate inside the female addition, cell proliferation response Megapodes are large mound [1], it extends no further than the of genital tissues to these signals was incubators from Australasia; they also proximate portion of the vagina. In similar in both groups. An alternative have a range of mating systems, but in contrast, the duck penis is a fully mechanism is for differential all species males build and defend the intromittent copulatory organ with cell-death/apoptosis to occur in the mound [14]. Some megapodes have a many remarkable features: it can developing chicken penis. Bone non-intromittent penis, while in at achieve prodigious lengths [6], morphogenic proteins (Bmps) are least one species (Leipoa ocellata)it sometimes longer than the known to be involved in apoptosis in is completely lost (Figure 1C) [5]. male himself [7], spirals in a mice genitalia [11]. Herrera et al. report The Phasianoidea superfamily (e.g., counterclockwise direction [1], and that indeed a derived pattern of Bmp chicken, quail and turkey) have features a unique explosive eversion expression results in reduction of non-intromittent penises [1], variable and insemination mechanism [8]. chicken genitalia via induced apoptosis body sizes, female incubation and According to Herrera et al., the in the distal end of the genital tubercle offspring care, and varied mating dramatically different copulatory starting at stage 36. Their study systems [14]. In the face of these organs in chickens and ducks share the demonstrates that Bmp4 and Bmp7 diverse life histories, the pleiotropy same early development. Both begin have different patterns of expression in hypothesis does not seem plausible, growing at embryonic stage 26 as the genital tubercle of chicken and as there is no obvious characteristic paired genital swellings between duck, but Bmp4 appears to be primarily shared only by these groups. However, the anterior and posterior cloacal responsible for apoptosis in the distal an intriguing possibility is that perhaps swellings. At stage 28, the paired cells of the chicken genital tubercle. By the timing of Bmp4 expression in the swellings merge to form a single determining that Bmp4 expression in chicken genital tubercle is dictated by tubercle with a sperm channel. The emu and alligator embryos (both have preventing pleiotropic effects of its tubercle continues to grow until stage fully intromittent penises) is virtually expression in other organ systems that 35 when it stops growing in chicks. identical to ducks, Herrera et al. may be developing earlier and that By stage 45, the chicken has barely a established that Bmp4 expression and also rely on Bmps (for example, the noticeable bump in the cloaca, while apoptosis in the distal genital tubercle limbs) [10,15]. If so, this may explain the duck has a well-developed phallus. evolved in chickens, rather than being why some birds end up with An important discovery made by lost in ducks. Further, functional non-intromittent penises that do Herrera et al. is that the mechanism experiments using Bmp antagonists not appear to offer a clear functional of external genital development is rescued the chicken penis from cell advantage, rather than completely evolutionarily conserved in birds death and regression, while activation losing the penis. and mammals. This allowed them to of Bmp signaling in ducks resulted Adaptive explanations of penis hypothesize that changes in gene in apoptosis of their genital tubercle, loss and reduction in birds include Dispatch R525 both natural and sexual selection similarly there may be more than one view of male sexual development. Nat. Rev. Genet. 7, 620–631. hypotheses. A reduced penis may developmental mechanism by which 10. Cohn, M.J. (2011). Development of the external increase copulatory efficiency if reduction of the penis has occurred. genitalia: conserved and divergent copulating becomes faster or easier, or Thanks to Herrera et al. we now have mechanisms of appendage patterning. Dev. Dyn. 240, 1108–1115. it may increase flight performance due one piece of the puzzle, but studying 11. Suzuki, K., Bachiller, D., Chen, Y.P., to weight reduction if the penis and the developmental mechanism of penis Kamikawa, M., Ogi, H., Haraguchi, Y., Ogino, Y., Minami, Y., Mishina, Y., Ahn, K., et al. (2003). associated machinery are heavy [2,3]. loss in Neoaves, and penis reduction in Regulation of outgrowth and apoptosis for the The penis may have been lost to tinamous and megapodes, would help terminal appendage: external genitalia: reduce the risk of acquiring sexually to complete the picture. The diversity development by concerted actions of BMP signaling. Development 130, transmitted diseases (STDs) that may of morphologies of bird genitalia 6209–6220. be common in birds [2,3]. Female suggests that evolution has likely 12. Sumoy, L., Wang, C.K., Lichtler, A.C., Pierro, L.J., Kosher, R.A., and Upholt, W.B. choice may have favored males with come up with more than one way (1995). Identification of a spatially specific reduced genitalia if these males were to lose the penis. enhancer element in the chicken Msx-2 gene less able to manipulate reproduction that regulates its expression in the apical ectodermal ridge of the developing limb and coerce females [2,3,16]. While buds of transgenic mice. Dev. Biol. 170, we lack sufficient data to rigorously References 230–242. 1. King, A.S. (1981). Phallus. In Form and Function 13. Davies, S.J.J.F. (2002). Ratites and Tinamous. test these hypotheses, preliminary in Birds, A.S. King and J. McLelland, eds. (New Tinamidae, Rheidae, Dromaiidae, Casuariidae, examinations have not yielded York: Academic Press), pp. 107–148. Apterygidae, Struthionidae (Oxford: Oxford universal support for any one of them 2. Briskie, J.V., and Montgomerie, R. (1997). University Press). Sexual selection and the intromittent organ of 14. del Hoyo, J., Eliott, A., and Sargatal, J., eds. [2,3,5,16]. However, there is no reason birds. J. Avian Biol. 28, 73–86. (1994). Order Galliformes. In Handbook to expect that all the independent penis 3. Montgomerie, R., and Briskie, J.V. (2007). of Birds of the World: New World Anatomy and evolution of copulatory Vultures to Guinea Fowl. Volume 2 reduction events in birds are the result structures. In Reproductive Biology and (Lynx Edicions). of the same selective pressures. Phylogeny of Birds. Part a: Phylogeny, 15. Merino, R., Rodriguez-Leon, J., Macias, D., Increased copulatory efficiency Morphology, Hormones and Fertilization, Ganan, Y., Economides, A.N., and Hurle, J.M. B.G.M. Jamieson, ed. (Science Publishers), (1999). The BMP antagonist Gremlin regulates may have been important for the pp. 115–148. outgrowth, chondrogenesis and programmed small Crypturellus if shorter 4. Herrera, A.M., Shuster, S.G., Perriton, C.L., and cell death in the developing limb. Development Cohn, M.J. (2013). Developmental basis of 126, 5515–5522. copulation — compared to the more phallus reduction during bird evolution. Curr. 16. Montgomerie, R. (2010). Sexual conflict and prolonged affair in their closest Biol. 23, 1065–1074. the intromittent organ of male birds. In relatives, Tinamus — resulted in less 5. Brennan, P.L.R., Birkhead, T., Zyscowski, K., The Evolution of Primary Sexual Characters Van deer, Waag, J., and Prum, R.O. (2008). in Animals, J. Leonard and A. Cordoba- predation. Reducing the incidence Independent evolutionary reductions of the Aguilar, eds. (Oxford University press), of STDs may have been important in phallus in basal birds. J. Avian Biol. 39, pp. 453–470. 487–492. 17. Brennan, P.L.R., and Prum, R.O. (2012). promiscuous species, such as 6. Brennan, P.L.R., Prum, R.O., McCracken, K.G., The limits of sexual conflict in the some megapodes and tinamous. Sorenson, M.D., Wilson, R.E., and narrow sense: new lessons from a Perhaps the reduction of the penis Birkhead, T.R. (2007). Coevolution of male and vertebrate system. Phil. Trans. R. Soc. 367, female genital morphology in waterfowl. PLoS 2324–2338. resulted from female choice for less ONE 2, e418. coercive males in some Galliformes 7. McCracken, K.G., Wilson, R.E., McCracken, P.J., and Johnson, K. (2001). Division of Organismal and Evolutionary if sexual conflict over forced Sexual selection: are ducks impressed by copulation was as rampant in their drakes’ display? Nature 413, 128. Biology and Department of Biology, last common ancestor as it is 8. Brennan, P.L.R., Clark, C., and Prum, R.O. University of Massachusetts Amherst, (2010). Explosive eversion and functional Amherst, MA 01003, USA. in modern waterfowl [6,17]. morphology of the duck penis supports sexual E-mail: [email protected] There may have been more than conflict in waterfowl genitalia. Proc. Biol. Sci. 277, 1309–1314. one ultimate reason why the penis 9. Wilhem, D., and Koopman, P. (2006). The was reduced or lost in birds, and makings of maleness: towards and integrated http://dx.doi.org/10.1016/j.cub.2013.04.035

Evolutionary Genetics: Inheritance of evolution and inheritance of complex adaptive traits, such as the a Complex Pollination Syndrome multicharacter floral syndromes that define pollinator interactions in plants, is an intriguing puzzle in evolutionary How adaptive traits that are controlled by multiple genes evolve is an intriguing genetics. question in evolutionary genetics. A recent study shows that tight linkage There have been numerous allows genes that contribute to a multitrait pollination syndrome to be inherited studies of the genetic basis of local together as a unit. adaptation and reproductive isolation among species. Complex adaptive Kevin M. Wright genes or combined effects in many traits have been found in several and Kirsten Bomblies independent loci? In the case of studies to be multigenic, rather than species that can hybridize, being caused by variation at single How do complex, multicomponent do appropriate trait combinations large-effect regulatory genes. In traits evolve? Does variation in such remain associated in the face of some cases, causal genes map traits arise due to changes at single gene flow? Understanding the together to inverted genomic regions