Advances in Sexual Selection Theory: Insights from Tropical Avifauna

ORNITOLOGIA NEOTROPICAL 19 (Suppl.): 151–163, 2008 © The Neotropical Ornithological Society

ADVANCES IN SEXUAL SELECTION THEORY: INSIGHTS FROM TROPICAL AVIFAUNA

Wendy P. Tori1, Renata Durães1, Thomas B. Ryder1, Marina Anciães2,8, Jordan Karubian3, Regina H. Macedo4, J. Albert C. Uy5, Patricia G. Parker1, Thomas B. Smith3,6, Adam C. Stein5, Michael S. Webster7, John G. Blake1, & Bette A. Loiselle1

1Department of Biology, University of Missouri-St. Louis and Whitney R. Harris World Ecology Center, 1 University Blvd., St. Louis, Missouri 63121-4400, USA. E-mail: [email protected] 2Natural History Museum and Biodiversity Research Center, University of Kansas, Lawrence, Kansas, USA. 3Center for Tropical Research, Institute of the Environment, University of California, Los Angeles, Box 951496, California 90095-1496, USA. 4Departamento de Zoologia, Universidade de Brasília, Brasília, DF, 70910-900, Brazil. 5Department of Biology, 108 College Place, Lyman Hall, Syracuse University, Syracuse, New York 13244, USA. 6Department of Ecology and Evolutionary Biology, University of California,Los Angeles, Box 951606, California 90095-1606, USA. 7School of Biological Sciences, Washington State University, PO Box 644236, Pullman, Washington 99164-4236, USA.

Resumen. – Avances en la teoría de la selección sexual: contribuciones de la avifauna tropical. – En los últimos 30 años, la selección sexual se ha convertido en una de las áreas de mayor crecimiento e influencia de la biología evolutiva y la ecología de comportamiento. La teoría de la selección sexual tiene efectos importantes en la evolución de las características de historia de vida, sistemas de cortejo y morfolo- gía, y ha sido sugerida como un factor que promueve la especiación. Las aves han jugado un rol esencial en su desarrollo. Sin embargo, la mayoría de estudios se han enfocado en especies de zonas templadas, a pesar que ellas comprenden menos de un cuarto de las especies de aves del mundo. Por lo tanto, antes de aplicar universalmente las teorías existentes, se recomienda cautela, especialmente considerando las tendencias latitudinales en las características de historia de vida y las estrategias evolutivas. Aquí, hemos seleccionado cinco estudios con aves tropicales que cubren diferentes aspectos de la teoría de la selección sexual. Dos estudios detallan los procesos evolutivos involucrados con signos de plumaje; uno de ellos estudia la influencia del “sensory drive” de las hembras en la evolución del plumaje de los machos, y el segundo investiga como la selección no azarosa de apareamiento puede promover la introgreción genética a lo largo de una zona de hibridación. Un tercer estudio examina como la diferencia de dieta entre sexos puede llevar a la asincronía temporal entre el periodo pico de actividad de despliegue de machos y el anidamiento de hembras. Un cuarto estudio detalla como diferencias en la estructura espacial de las asambleas ______8Current address: Bird Collection, Instituto Nacional de Pesquisas da Amazônia – INPA, Av. André Araújo 2936, Petrópolis, Manaus-AM 69060-001, Brazil.

151 TORI ET AL. de cortejo y la organización social influencian el grado de sesgo reproductivo de machos saltarines. El quinto estudio examina las diferencias en la intensidad de selección sexual en taxones de zonas templadas y tropicales, y evalúa, entre regiones, nuestro conocimiento actual sobre la frecuencia de la paternidad extra- pareja. Se discuten las contribuciones de estos estudios a nuestro entendimiento actual de la selección sexual. Abstract. – Over the last 30 years, sexual selection has become one of the most influential and rapidly growing areas within evolutionary biology and behavioral ecology. Sexual selection has important effects on the evolution of life history traits, mating systems and morphology, and also has been suggested as a factor that promotes speciation. Avian systems have played an essential role as models in the development of sexual selection theory. However, most studies have focused on temperate species, although they account for less than one quarter of avian species worldwide. Therefore, before applying existing theories universally, caution is advised, especially considering latitudinal trends in life history traits and evolutionary strategies. Here, we brought together five tropical bird studies covering different aspects of sexual selection theory. Two studies detail the evolutionary processes involved with plumage signals; one of these deals with the influence of female sensory drive on the evolution of male plumage, and the second investigates how non-random female mate choice can promote genetic introgression along a hybrid zone. A third study examines how sex differences in diet can lead to temporal asynchrony between periods of peak male display activity and female nesting. A fourth study details how differences in lek spatial structure and social organization influence the degree of male reproductive skew among manakins. The fifth study examines differences in the intensity of sexual selection in temperate and tropical taxa and assesses current knowledge regarding the frequency of extra-pair paternity among regions. The contributions of these studies to our current understanding of sexual selection are discussed. Accepted 14 October 2007. Key words: Extra-pair paternity, hybridization, lekking, mate choice, reproductive skew, sexual selection, tropical birds, tropical-temperate comparisons, visual signals.

INTRODUCTION of one sex (usually females) drive evolution of traits in the opposite sex through non-ran- Since initially proposed by Charles Darwin dom mate choice. Establishing the relative (1859, 1871), the theory of sexual selection importance of such intra- and inter-sexual has generated considerable interest and con- components in empirical studies is often diffi- troversy among evolutionary biologists. cult and complicated by the interaction Broadly speaking, sexual selection theory between these two processes. concerns the evolution and selection of traits Over the last 30 years, sexual selection that affect mating success (Andersson 1994). theory has become one of the fastest develop- Elaborate and often costly phenotypic traits ing areas in evolutionary and behavioral ecol- are hypothesized to arise through differences ogy (Gross 1994). Sexual selection is now in reproductive success as a function of com- recognized as an essential evolutionary factor petition for mates. This variance in reproduc- shaping behavior, morphology, life history, tive success is promoted by two distinct and mating systems, both in animals and selective processes. The first is the intra-sex- plants (Searcy 1982, Andersson 1994), and ual component of sexual selection, which can also be an important force driving specia- results from direct competition among indi- tion (Lande 1981, Ptacek 2000, McDonald et viduals of the same sex (usually males) for al. 2001, Stein & Uy 2006). Birds have played mates. The second is the inter-sexual compo- a central role as subjects for the study of sex- nent of sexual selection, in which individuals ual selection. However, the vast majority of

152 SEXUAL SELECTION THEORY: INSIGHT FROM TROPICAL BIRDS birds that have been studied are from the tem- examines how variation in spatial structure perate zone. Temperate species comprise less and social organization in the family Pipridae than 25% of all bird species worldwide (Mar- influence the intensity of sexual selection as tin 2004), and among passerines, 80% measured by male reproductive skew. The (~4000) of species are in the tropics (Stutch- fifth study reviews our current knowledge bury & Morton 2001). This begs the question about differences in the frequency of extra- of whether the important findings we are rap- pair copulation among tropical and temperate idly accumulating in the field of sexual selec- avian species and possible explanations for tion are universally applicable or not. such differences. Although the current lack of data on tropical species makes comparisons difficult, there are PLUMAGE CONSPICUOUSNESS IN reasons to be wary before directly applying DISPLAYING MANAKINS (PIPRIDAE) concepts developed from studies of temper- FROM THE ILICURA–CORAPIPO ate species to tropical systems. For example, CLADE: A COMPARATIVE TEST OF several life history components are known to THE SENSORY DRIVE HYPOTHESIS show latitudinal variation (e.g., Martin 1996, Martin et al. 2000, Ghalambor & Martin Sexual selection by female choice has pro- 2001), and we can expect that differences in moted the evolution of exaggerated male phe- characteristics such as survival, investment in notypes among lekking birds (Kirkpatrick & reproduction, territoriality, breeding syn- Ryan 1991, Anderson 1994). However, com- chrony, and frequency of extra-pair paternity peting hypotheses suggest different roles for will lead to variation in the opportunity for how ecological specializations act on mate sexual selection. choice, and ultimately shape the evolution The diversity of mating systems and com- of male phenotypes, both morphological plex social behaviors observed among tropical and behavioral (Prum 1997). Among them, species presents excellent opportunities to sensory drive (Endler & McLelland 1988) develop model systems for both empirical and predicts the evolution of conspicuous pheno- theoretical sexual selection research. Here, we types because of reduced costs associated outline five examples of current research on with mate search. In order to evolve by sen- tropical birds, and discuss how these studies sory drive, signals should be produced within have contributed to a more general under- sensory conditions that favor conspicuous- standing of sexual selection among lekking ness. Among polygynous lekking birds, the and socially monogamous species. Two stud- hypothesis predicts that males should display ies examine how sexually selected signals in in light conditions at display sites, and at non- the family Pipridae are driven by signal per- random subsets of sites within the habitat, ception in variable habitats via sensory drive that favor signal detection by females; and in the Illicurinii tribe and by genetic introgres- that females should visit males displaying sion and frequency-dependent female choice under light environments that favor detection. in the Manacus clade. A third study explores These predictions were tested among five how sex-related differences in diet may cause closely related species within the manakins temporal asynchrony between male courtship from the Ilicura-Corapipo clade [Pin-tailed behavior and female nesting in Long-wattled Manakin (Ilicura militaris), White-throated Umbrellabirds (Cephalopterus penduliger), and Manakin (Corapipo gutturalis), White-ruffed discusses the potential role for leks as infor- Manakin (Corapipo leucorrhoa), Pacific White- mation exchange centers. A fourth study ruffed Manakin (C. heteroleuca), White-bibbed

153 TORI ET AL.

Manakin (C. altera), and Golden-winged more contrasting during all light categories Manakin (Masius chrysopterus)]. used for displays, when compared to periods Visual signals produced by males during without displays at display sites. Moreover, displays were modeled based on ambient light the Pin-tailed Manakin, White-bibbed (Endler 1990, 1993) and plumage spectra Manakin and Pacific White-ruffed Manakin measured with spectrometers (Ocean Optics, display sites provided light conditions Inc.) in the habitat of studied populations and that increased contrast in comparison to from captured individuals and museum speci- light conditions measured at sites not used mens, respectively. Female sensory systems for displays (i.e., non-display sites). Female were modeled with estimates of spectra sensi- visits, however, were not more frequent tivities based on the opsin genes sequenced during displays in ambient light conditions for the species, following Ödeen & Håstad of increased male plumage contrast, in com- (2003), and on the likely composition of parison to the average contrast of male dis- carotenoids present in the oil droplets from plays. the cone photoreceptors found in bird retinas Our results indicate that the behavioral (Goldsmith et al. 1984, Goldsmith & Buttler novelty observed in the White-throated 2003). Contrast was estimated for both Manakin – a male preference for displaying close (within plumage contrast) and far under sunny conditions (Endler & Théry (between plumage and background) distances, 1996, Anciães & Prum in prep.) – is associ- based on modeled thresholds from the recep- ated with a new sensory environment avail- tor-noise model equations (Vorobyev & Oso- able for the species (Anciães & Prum in prep.) rio 1998). Within plumage contrasts were and corresponds to an increase in plumage estimated and compared using the LSED- contrast within the studied population. How- MRPP method (Mielke & Berry 2001, Endler ever, these associated changes were preceded & Mielke 2005), and contrasts between plum- by the evolution of the glossy blue-black age and background were estimated in values plumage typical of the genus, which arose of just noticeable differences (Osorio & in the ancestor of Corapipo, indicating that Vorobyev 1986, Vorobyev et al. 1998, Siddiqi this plumage has not evolved for conspicu- et al. 2004, Eaton 2005), compared through ousness. Furthermore, plumage contrast nonparametric and parametric analyses of was highly decreased in Corapipo when com- variance. pared to the other species from the clade, Ili- Our results support a role of sensory drive cura and Masius, either in their own habitat or in the evolution of conspicuous male pheno- in simulations using the ambient light avail- types within populations, based on chromatic able to the other species, indicating that yel- contrast during male displays in all species, low and red plumages are more contrasting and on achromatic contrasts in the White- under any of the light environments sampled throated Manakin, suggesting that changes here, which are mainly green even during in behavior enhanced signal conspicuity. cloudy conditions. Lastly, the data indicate More specifically, all species but the Pin-tailed a weak association between changes in Manakin showed increased within-plumage plumages and ambient light among species an contrast or contrast between plumage and a strong correlation between sensory environ- background in the light category most used ments and ecological niches (Anciães during male display (i.e., cloudy, shade, 2005), showing considerable plumage differ- sunny gaps). In the case of the Pin-tailed entiation among species with relative similar Manakin, the within-plumage contrast was ecologies.

154 SEXUAL SELECTION THEORY: INSIGHT FROM TROPICAL BIRDS

SEXUAL SELECTION AND THE tion, we used a spectrophotometer to measure DYNAMICS OF DISPLAY TRAIT the color properties of male plumage, the INTROGRESSION ACROSS HYBRID visual background and the ambient light at the ZONES hybrid zone, and at pure golden and white populations. This allowed us to determine if a Hybridization among individuals from dis- variable visual habitat can influence the attrac- tinct species typically results in less fit tiveness and hence the patterns of yellow offspring but it can also be a creative evolu- plumage introgression. tionary process by acting as a conduit for the We found that yellow males had signifi- exchange of novel traits between populations cantly higher mating success than white males (Anderson & Stebbins 1954). When under- at mixed leks, suggesting that sexual selection standing the origin of elaborate traits and favoring yellow males drives the unidirectional female preferences, studies often assume that spread of yellow plumage across the Manacus the trait and preference emerge within the hybrid zone (Stein & Uy 2006). In addition, population and eventually reach fixation (see we found that yellow and white males did not Andersson 1994). Alternatively, display traits differ in body size, position in leks and levels and female preferences may have originated of aggressiveness, suggesting that male-male from another population and spread second- competition cannot explain the yellow male arily into a given population. Although this mating advantage. However, we found that does not address the ultimate origin of a trait females visited both yellow and white males, and preference, it does provide a mechanism and rejected white males for yellow males. for the evolution of elaborate displays and This suggests that the yellow male mating preferences for a given population. advantage may be driven by female preference The closely related Golden-collared for yellow males. (Manacus vitellinus) and White-collared (M. can- The yellow male mating advantage is large. dei) manakins form a hybrid zone character- Yellow plumage is therefore expected to ized by several concordant genetic and sweep through the white-collared population; morphometric clines centered near Rio however, the plumage cline seems stable near Robalo in Western Panama. A cline for yellow Rio Changuinola. This suggests that some plumage, however, is displaced by 50 km to factors may be constraining its rapid spread. the west, into the white-collared population, We found that at least two factors may slow where it forms a similar steep cline near Rio the rate of trait introgression. First, we found Changuinola (Brumfield et al. 2001). Adult that the yellow male mating advantage only males in the 50 km region between Rio occurs in mixed leks where yellow males are Robalo and Rio Changuinola therefore carry in high frequencies. At the leading edge of the predominantly white-collared alleles but look plumage cline, yellow males are rare and so similar to Golden-collared Manakins due to would not experience a significant mating the introgressed yellow plumage (Brumfield et advantage over white males until they reach al. 2001). higher frequencies, thus slowing the spread of At the edge of the plumage cline, yellow- yellow plumage into the white population and white-collared males form common mat- (Stein & Uy 2006). Second, as measured by ing arenas (“mixed leks”). We monitored yel- the perceived difference in color between low and white males in these mixed leks to male plumage and the visual background, we determine the underlying mechanisms that found that yellow plumage appears more con- favor the spread of yellow plumage. In addi- spicuous than white plumage in the hybrid

155 TORI ET AL. zone and allopatric golden-collar habitats, Long-wattled Umbrellabirds aggregate in leks while white plumage appears more conspicu- to display to females but provide no parental ous than yellow plumage in the allopatric care (Jahn et al. 1999, Karubian et al. 2003), white-collared habitat (Uy & Stein 2007). This suggesting that the opportunity for sexual pattern suggests a mechanism for the unidi- selection may be high. In our study popula- rectional spread of yellow plumage across tion in Bilsa Biological Station, northwestern the hybrid zone but slowed movement Ecuador (Berg et al. 2000), we found that beyond it. males were approximately 1.5x larger than The role of hybridization as a source of females and had wattles and crests approxi- genetic variation for adaptive traits has long mately four times larger than those of been appreciated (e.g., Grant & Grant 1994), females. Variance in these traits was similar but its potential role in the evolution of elabo- between the sexes. Juvenile males spent at rate display traits is relatively unexplored. least one year with crests, wattles, and body Given that over 10% of avian species hybrid- size intermediate between adult males and ize with little to no costs (Grant & Grant females. 1992), hybridization can be important in the Lek size ranged from 1–15 males, and origin of novel display traits. males exhibited at least two strategies during the breeding season. Some males (usually 5– LEK DYNAMICS AND SEXUAL 10 per lek) held fixed territories while other SELECTION IN THE LONG- “floating” males moved between leks without WATTLED UMBRELLABIRD holding territories. These floating males may have been younger, competitively inferior In lek breeding species, males and females males moving in response to spatial and tem- follow dramatically different reproductive poral variation in fruit availability. Territorial strategies. Typically, males defend territories males were observed departing and returning on leks and attempt to attract multiple mates to leks in a coordinated manner and foraging whereas females focus on nesting and paren- in groups away from leks. One un-tested pos- tal care (Wiley 1991, Höglund & Alatalo sibility is that leks may serve some role in 1995). This leads to a very different set of information-sharing as well as mate choice. In evolutionary pressures on the sexes and is the this sense, individuals may find patchily-dis- primary cause of the behavioral and morpho- tributed food resources by following other logical sexual dimorphism typical of lek- males when leaving the lek (Wagner & breeding species (Andersson 1994, Dunn et al. Danchin 2003). 2001). The ecological implications of these Lek activity was strongly seasonal. Num- sex-related differences, however, are less well ber of males at the lek, average song rate, and understood. Here, we provide an overview of rate of female visitation were highest during lek dynamics of the Long-wattled Umbrella- the dry season (August–December), whereas bird, with special emphasis on the potential the period of lowest lek activity corresponded implications of ecological and behavioral vari- to the wettest part of the year. Even during ation between the sexes. periods of lowest lek activity, however, at least Long-wattled Umbrellabirds are large, fru- some males were present at each lek. Surpris- givorous birds endemic to the humid Chocó ingly, most female nesting occurred when lek rain forests of northwestern Ecuador and activity was at its lowest, leading to a temporal western Colombia (Snow 1982). As with disconnect between activity at leks and female many members of the family Cotingidae, male nesting (which peaked six months after peak

156 SEXUAL SELECTION THEORY: INSIGHT FROM TROPICAL BIRDS lek activity). This incongruous pattern may be tics (e.g., dominance, Foster 1983). Sexual driven by the fact that males and females track selection theory suggests that, when given a different resources. Males may rely on fruit to choice, females may maximize their fitness by maintain the physiological state required for mating preferentially with high quality males energetically costly song and displays at the (Andersson 1994, Höglund & Alatalo 1995, lek, whereas females may rely on insects for Shuster & Wade 2003). To do so, females nesting, egg production, and provisioning of must have the opportunity to assess potential the young. Consistent with this idea, we found mates. The degree of temporal synchrony and that males ate more fruit than did females, spatial overlap among sexes constrains female and that male fruit consumption during low access to males, and has potential implications lek activity periods was approximately one- for male reproductive skew. Moreover, social half that of high lek activity periods. A further organization of males (e.g., dominance hierar- prediction, which remains to be tested, is that chies) may have repercussions on male mating fruit availability will be highest during periods success by limiting female choice (Foster of high lek activity, while insect abundance 1983). will peak concurrently with female nesting. In this study, we examined spatial and How the birds manage to fertilize eggs social factors that may influence reproductive and reproduce given this unusual asynchrony skew for three co-occurring lekking manakin between lek activity and nesting is an open species: the Wire-tailed Manakin (Pipra fili- question. Females may be capable of storing cauda), the Blue-crowned Manakin (Lepidothrix male sperm for long periods of time. Alterna- coronata), and the White-crowned Manakin tively, only a subset of the fittest males may be (Pipra pipra). These species share many eco- able to maintain year-round presence at the logical (e.g., diet) and morphological traits lek sites, and it is during periods of lowest lek (e.g., body size, sexual plumage dichroma- activity that these males monopolize matings tism). Moreover, they overlap broadly in their with females. breeding period and, thus, are expected to show few inter-specific differences in tempo- SPATIAL STRUCTURE AND SOCIAL ral factors. In contrast, these manakins differ ORGANIZATION OF MANAKINS: in spatial structure and social organization POTENTIAL IMPLICATIONS FOR (Loiselle et al. 2007), making them ideal for a MALE REPRODUCTIVE SKEW study on the effects of these factors on reproductive skew. Here, we specifically examined Lekking is a promiscuous mating system in the effects of three factors, with the following which males congregate in display arenas that predictions: 1) Female crowding, measured as females visit to mate. Males do not provide the degree of female spatial aggregation: spe- parental care and do not monopolize cies with clumped female dispersion were pre- resources essential to females. This leads to dicted to have higher reproductive skew strong sexual selection and variance in male- because males will have differential access to mating success (hereafter male reproductive females depending on where their territories skew). The degree of male reproductive skew are located in relation to the areas of high is hypothesized to vary as a function of tem- female concentration; 2) Male encounter rate, poral (e.g., female breeding synchrony, measured as the proportion of males in the Shuster & Wade 2003), spatial (e.g., female population potentially encountered by crowding, Schuster & Wade 2003, inter-lek females: in species with greater male encoun- spacing, Foster 1983), and social characteris- ter rate, females have the ability to compare

157 TORI ET AL. and assess a greater number of mates (assum- male reproductive skew. Species differed in ing females have similar mating preferences, degrees of reproductive skew and those diffe- certain males will have higher reproductive rences matched our overall prediction. In par- success than others leading to high reproduc- ticular, male encounter rate by females and tive skew); 3) Dominance, measured as the dominance were the two factors that best degree of male associations and the presence explained skew differences between species. of dominance hierarchies among males: in Further studies are needed to differentiate the species with dominance hierarchies, top-rank- relative importance between these two fac- ing males may control access to females and tors. In a broader context, our results provide are expected to have higher reproductive suc- information about how population-level process than subordinate males, thus increasing cesses have the potential to influence the reproductive skew. variance in male reproductive success, and Male mating success was measured using ultimately the direction and strength of sexual microsatellite paternity analyses based on selection. DNA collected from chicks and mothers at nests and from potential fathers at leks. SEXUAL SELECTION AND Reproductive skew was measured using λ MONOGAMY IN TROPICAL index (Kokko & Lindström 1997) and bino- AND TEMPERATE BIRDS mial skew index (Nonacs 2000). Species were ranked according to their degree of female Many socially monogamous bird species are crowding (i.e., spatial overlap using Moran’s I, subject to strong sexual selection, a fact that Moran 1950), male encounter rate and domi- has baffled biologists since Darwin (1871). nance; reproductive skew predictions were Evidence is mounting that extrapair paternity generated based on these factors. The Wire- (EPP) are common in socially monogamous tailed Manakin had relatively low levels of species (reviewed in Griffith et al. 2002) and female crowding, intermediate male encoun- can potentially generate strong sexual selec- ter rates, and facultative associations among tion (Webster et al. 1995). However, the vast males (strongest association among the three majority of this evidence comes from studies species). The White-crowned Manakin had an of temperate zone species, yet 80% of all pas- intermediate degree of female crowding, serine birds are tropical. Indeed, it has been intermediate male encounter rate and a loose suggested that EPC are uncommon and association among males. The Blue-crowned therefore unimportant to sexual selection in Manakin had a low degree of female tropical birds (Stutchbury & Morton 2001). crowding, low male encounter rate and the Thus, we face two important questions with weakest association among males. Given regard to the role of EPP in sexual selection: these spatial and social characteristics, our is EPP less common in the tropics than in the overall prediction (including the three factors) temperate zone? And, if so, what drives sexual was that the Wire-tailed Manakin should have selection in tropical monogamous species? the highest reproductive skew, followed by Three lines of evidence have been used to the White-crowned Manakin; the Blue-crow- suggest that EPP is less important to sexual ned Manakin was predicted to have the lowest selection in tropical monogamous systems, reproductive skew. but each has problems. First, testes size is Our results generally supported our pre- thought to be positively associated with rates dictions as we found a relationship between of EPP (Møller & Briskie 1995, Dunn et al. the targeted spatial and social factors and 2001) and some studies have indicated that

158 SEXUAL SELECTION THEORY: INSIGHT FROM TROPICAL BIRDS tropical species generally have smaller testes important to the sexual selection process for than temperate species (Stutchbury & Morton at least some tropical species. Both of these 2001), thus suggesting that tropical birds have species exhibit high EPF rates (Red-backed low rates of EPP. However, the relationship Fairywrens: 51.1% of 514 nestlings sired by between testes size and EPP rates is unclear extra-pair males; Blue-black Grassquit: 50% (Calhim & Birkhead 2007), and other studies of 20 nestlings) and a highly skewed distribu- have indicated that there is no latitudinal tion of male reproductive success. Moreover, trend in testes size (Dunn et al. 2001, Pitcher et the relationship between total male reproduc- al. 2005). Second, the breeding synchrony tive success and number of extra-pair mates hypothesis (Stutchbury & Morton 2001), (i.e., the “Bateman gradient”) was strongly which posits a positive relationship between positive for both species, with number of breeding synchrony and rates of extrapair mates accounting for 71% (Fairy-wrens) and paternity, suggests lower EPP rates in the 57% (Blue-black Grassquits) of the total vari- tropics because, in many cases, tropical birds ance in male reproductive success. These breed less synchronously than do temperate cases illustrate that EPP can be high in tropi- birds. However, the effects of breeding syn- cal birds, and we suggest that sexual selection chrony are controversial and may not be asso- can operate via different mechanisms in many ciated with EPP rates (Saino et al. 1999, tropical species. Yezerinac & Weatherhead 1997). Finally, some Thus, more data are needed before we can genetic studies of tropical birds have shown draw general conclusions about the mecha- low EPP rates, and this has been extrapolated nisms of sexual selection in monogamous to a conclusion of generally low rates of EPP birds. If EPP is indeed rare in tropical birds, in tropical species (Stutchbury & Morton then a comparison of tropical to temperate 2001). However, to date data are available for species should yield important insights into only seven tropical species, of which three the ecological factors leading to variation in show no EPP, three exhibit rates of 8 to 15% EPP rates, such as breeding synchrony or of the brood, and one species exhibits a high migration (reviewed in Petrie & Kempenaers rate of EPP (Stutchbury & Morton 2001). 1998 and Griffith et al. 2002). Moreover, a We do not want to reject the possibility generally low frequency of EPP in the tropics that EPP is rare in tropical birds, but we would suggest that sexual selection operates would like to challenge this view. We believe via different mechanisms in the temperate that a first crucial step would be to critically zone and in the tropics, and this might have assess the assumptions (e.g., breeding syn- important implications for the sort of sexual chrony hypothesis) and data (e.g., EPP rates, signals that might have evolved. In contrast, if testes size) underlying the concept that EPP EPP is as common in the tropics as it is in the in tropical birds is rare. Additionally, the ques- temperate zone, then there may be a common tion of whether tropical birds have EPP rates and general mechanism driving the process of similar to that of temperate birds, and sexual selection in monogamous systems whether EPP in these birds contributes to across latitudes. sexual selection are issues that can only be resolved with more data. Our studies of two CONCLUDING REMARKS tropical and socially monogamous species, the Red-backed Fairywren (Malurus melanocephalus) In 1871, Darwin introduced the concept of and the Blue-black Grassquit (Volatinia jaca- sexual selection to describe differences in rina) show that extrapair copulations are morphological and behavioral characteristics

159 TORI ET AL. among individuals that could have an impact shown to display at sites and under light con- upon their reproductive success. Since then, ditions that heightened plumage contrast and the study of sexual selection has come a long supposed detection by females, such behavior way, theoretically and empirically, despite the did not always result in more female visits. fact that many of its core concepts remain Failure to find increased female visitation unchanged (Andersson 1994). The tropics, under favorable light conditions does not nec- with its incredible diversity of species, com- essarily indicate that plumage contrast is not plex social behaviors and mating systems, an important cue in female choice. Rather, provide exceptional opportunities to conduct female visits may be influenced by spatial research and increase our current knowledge overlap of females with male display sites and of sexual selection. In this symposium, we attractive males may be located at sites that brought together five examples of current intercept few females. Moreover, population- research on tropical birds to examine what level analyses of variance in male reproductive insights tropical taxa provide to sexual selec- success showed that spatial and social aspects tion theory. These studies make four general of lek organization are important factors contributions to our current understanding of influencing female choice, male reproductive sexual selection. success and, ultimately, the strength of sexual First, they shed light on the origins and selection. evolution of exaggerated male display, a topic Third, one study demonstrated that sexual that has been controversial for a long time. selection also operates, and can be a strong Two studies provided evidence that male dis- evolutionary force, in socially monogamous play traits evolved in response to environ- birds. Data are currently limited, but it is clear mental conditions and one of them that that this is true for at least some tropical spe- display traits can originate via hybridization. cies as well as for temperate species. While These findings are important because they extra-pair paternity suggests that, even in reveal two potential mechanisms that may monogamous systems, females may have rela- play an important role in the evolution of the tively free choice of mating with multiple spectacular diversification of male secondary partners, in reality female mating options may sexual traits in the tropics. be limited by male behaviors (e.g., male guard- Second, these studies demonstrated that a ing) and also by ecological factors (e.g., breed- single trait rarely is implicated as the sole fac- ing synchrony). The extent to which these tor that explains female choice. Rather, mate factors can account for variation in EPP rates choice is demonstrated to be context-depen- across species remains an open question, and dent where selection on particular traits may comparisons of tropical species in different differ or be constrained by environmental or environments, as well as between tropical and social context. For example, environmental temperate species, should be revealing. features, such as insect abundance, may affect Fourth, these studies demonstrated how female reproductive behavior in umbrella- recently developed methods and equipment birds, while fruit abundance may influence are now used to characterize sexually-selected male display activity at leks. Further, environ- traits in biologically meaningful ways, and are mental features at leks appear to influence helping to advance our understanding of contrast in male plumage, and thus determine female choice and its impact on male repro- whether Yellow- or White-collared Manakin ductive variance and sexual selection. Pater- males are preferred by females. Although nity analysis using molecular markers has males of three other manakin species were become increasingly important to provide

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