ORNITOLOGIA NEOTROPICAL 23: 261–274, 2012 © The Neotropical Ornithological Society

THE IMPORTANCE OF SUBOSCINE AS STUDY SYSTEMS IN ECOLOGY AND EVOLUTION

Joseph A. Tobias 1, Jeff D. Brawn 2, Robb T. Brumfield 3, Elizabeth P. Derryberry 3, Alexander N. G. Kirschel 1,4, & Nathalie Seddon 1

1Edward Grey Institute, Department of Zoology, University of Oxford, UK 2Department of Natural Resources and Environmental Sciences, University of Illinois, Urbana, Illinois 61801 USA 3Museum of Natural Science and Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803 4Department of Biological Sciences, University of Cyprus, PO Box 20537, Nicosia 1678, Cyprus

Resumen. – La importancia del uso de Suboscines como sistema de estudio en ecología y evolución. – Las aves Suboscines son uno de los componentes más prominentes de la avifauna Neotropical, sin embargo aun son relativamente poco estudiados en comparación a su clado hermano, los Oscines. Esta situación parece estar cambiando rápidamente debido a que los ornitólogos se han dado cuenta que los suboscines ofrecen un sistema ideal de estudio para investigar una variedad de preguntas. Resumimos los resultados de un simposio enfocado en estudios de suboscines traqueofonos (trepapalos, furnáridos, hormigueros y afines) y destacamos avances recientes en nuestro entendimiento de su historia natural y comportamiento. Argumentamos que debido a su antigüedad y altos niveles de diversidad, ellos son un excelente modelo para análisis comparativos y filogenéticos. Sobre todo, muchos de los detalles de su reproducción y comunicación los predisponen a que se realicen obser- vaciones de campo y estudios experimentales de interacciones sociales y de evolución de las señales, así como a técnicas de reconocimiento vocal. Discutimos potenciales líneas de investigación futuras en suboscines, y con- cluimos que estas especies van a jugar un rol importante como sistema de estudio en ecología tropical y evolución. Abstract. – Suboscine birds are one of the most prominent components of Neotropical avifaunas, yet they remain relatively poorly studied in comparison with their sister-clade, the oscine . This situation appears to be changing rapidly as more ornithologists realize that suboscine birds offer ideal study systems for investigating a variety of research questions. We summarise a symposium focused on studies of tracheophone suboscines (woodcreepers, , and allies) and highlight recent advances in our understanding of their history and behavior. We argue that because of their antiquity and high levels of diversity, they make excellent subjects for comparative analyses and phylogenetic models. Moreover, several details of their breeding and signaling systems predispose them to field-based observational and experimen- tal studies of social interactions and signal evolution, as well as automated techniques for vocal recognition. We discuss potential new avenues of research on suboscine passerines, and conclude that they are likely to play an increasingly important role as study systems in tropical ecology and evolutionary biology. Key words: suboscine, ecology, evolution, signaling

Suboscine birds account for over 10% (ϳ1150 received remarkably little research attention in species) of global diversity, and around a comparison with their sister-clade, the oscine ÀIWKRISDVVHULQHGLYHUVLW\7KH\KDYHUDGLDWHG passerines, which abound in the temperate to a spectacular extent in the Neotropics, which zone. A preliminary survey of the literature is home to all but a handful of suboscine reveals that 202 articles published since 1926 species (Ricklefs 2002). Despite this, they have contain “suboscine” in the title or abstract

261 TOBIAS ET AL.

FIG. 1. Increasing rate of publication for papers focused on suboscines, since 1926 (data binned into 5-year periods). Totals are numbers of papers containing the word “suboscine” in title, abstract or keywords ex- tracted from Web of Knowledge. We do not make a direct comparison with oscines because most papers focusing on suboscines tend to highlight the fact, whereas those focusing on oscines do not.

(see Fig. 1). This may appear substantial, but sometimes referred to as the non-tracheo- it contrasts markedly with the 17,852 papers phone (or “bronchophone”) suboscines, a published in the same period containing the FODGHSULPDULO\FRQVLVWLQJRI W\UDQWÁ\FDWFKHUV word “passerine” and excluding the word (Tyrannidae), (Pipridae) and “suboscine”. A small proportion of this larger (Cotingidae), has received the most attention. total is made up of general studies, which Conversely, the infraorder Furnariides, i.e. potentially include at least some data from tracheophone families such as the antbirds suboscines, but the vast majority is focused (Thamnophilidae) and ovenbirds (Furnariidae), VSHFLÀFDOO\RQRVFLQHV,QGHHGWKHWUXHUHVHDUFK has traditionally been largely ignored. The output based on oscine systems is far higher historical emphasis on Tyrannides has occurred than these calculations imply as much of it is in part because several lineages colonized the published without noting the word “passerine”, temperate zone, breeding as far north as the including many thousands of papers on high- United States and Canada. Moreover, tropical SURÀOH PRGHO V\VWHPV VXFK DV *UHDW 7LWV forms such as manakins and cotingas are (Parus major), Red-winged Blackbirds (Agelaius often highly charismatic, with extreme sexual phoeniceus) and Zebra Finches (Taeniopygia guttata). dimorphism and extravagantly ornamented Further research biases exist within males. In contrast, tracheophone suboscines the subsocines. The infraorder Tyrannides, are absent from the temperate zone, and tend

262 THE IMPORTANCE OF NEOTROPICAL SUBOSCINE BIRDS AS STUDY SYSTEMS IN ECOLOGY AND EVOLUTION to be overlooked even in the tropics because local and regional variation in vocalizations WKH\DUHSHUFHLYHGDVGXOORUGLIÀFXOWWRVWXG\ (e.g. individual repertoires, dialects), such that (Remsen 2003). mechanisms of ecological or social selection The situation has changed rapidly DUH GLIÀFXOW WR GLVHQWDQJOH IURP FXOWXUDO over recent years as a growing number of evolution (Tobias et al. 2010b). researchers have realized that tracheophone 6LPLODUO\ WKH ÀQGLQJ WKDW PDQ\ RVFLQH suboscines make ideal research subjects for JURXSVKDYHKLJKOHYHOVRI SOXPDJHUHÁHFWDQFH a number of practical reasons. First, they are in ultra-violet (UV) wavelengths, as well as ecologically diverse, occurring in all major visual sensitivity to such wavelengths, suggests habitats from humid lowland tropical forests to that the use of human vision to assess plumage the snowline. Second, they are socially diverse, colors and contrasts is invalid (Eaton 2005). spanning a variety of breeding systems from Human vision is insensitive to UV wavelengths social monogamy to cooperative breeding. and thus numerous previous studies have Third, they are typically highly responsive to overlooked cases of signal divergence or tape playback, making them relatively easy to cryptic dichromatism in oscine birds (Bleiweiss catch in mistnets, and therefore to measure, 2004, Eaton 2006). These problems are color-band, radio-tag, blood-sample and so negligible in tracheophone suboscines as their on (Bard et al. 2002). It also means that they plumage generally has very low levels of UV are amenable to playback experiments. Fourth, UHÁHFWDQFHDQGWKHVSHFWUDOVHQVLWLYLW\RI WKHLU many species of suboscines are fairly common, visual systems is not tuned to UV wavelengths ORXGDQGFRQVSLFXRXVHYHQLQKXPDQPRGLÀHG (Seddon et al. 2009). This means that environments. This means that it is relatively suboscine clades are amenable to comparative HDV\WRÀQGDQGIROORZWKHPIRUWKHSXUSRVH analyses based on simple visual comparison of observational studies, and to record their of plumage colours and contrasts, rather than vocalizations. Thus, it is possible to build up the use of colour spectrophotometry coupled VXIÀFLHQWVDPSOHVL]HV LQWHUPVRI QXPEHUV with visual modelling (e.g. Seddon et al. 2008). of individuals) for statistical tests an important Another aspect that has drawn researchers consideration given that many tropical species to the tracheophone suboscines is the are found at lower population densities than contrasting perspective they provide on a their temperate-zone counterparts (Tobias et number of long-standing questions (Ricklefs al. 2012b). 2002). In particular, they offer unparalleled The signaling systems of tracheophone systems for studying the evolutionary suboscines also offer intrinsic practical implications of ‘slow’ life history strategies. advantages for biologists. For example, it is well Most members of this clade are characterized known that their vocalizations are relatively by classic tropical social systems involving simple and stereotyped (Kroodsma 1984, convergent sex-roles, long-term pair-bonds Morton 1996, Lindell 1998), thus facilitating and year-round territoriality (Greenberg & acoustic analyses used in tests of evolutionary Gradwohl 1983, Kirschel et al. 2011, Tobias et theory (e.g. Seddon 2005) and speciation (e.g. al. 2011). As a corollary, they also tend to be Seddon & Tobias 2007, Seddon et al. 2008), as extremely sedentary (Greenberg & Gradwohl well as analyses of geographic variation (Ippi 1997, Woltmann et al. 2012), with delayed natal et al. 2011) and criteria for assessing species dispersal and highly stable territorial networks limits (Isler et al. 1998, Tobias et al. 2010a). (Greenberg & Gradwohl 1986, Kirschel et This contrasts with many oscine taxa in which al. 2011). Overt evidence of sexual selection song learning is prominent, leading to complex such as polygyny and extra-pair fertilizations

263 TOBIAS ET AL. appears to be rare (Fleischer et al. 1997), Ricklefs 2006, Seddon et al. 2008, Claramunt although divorce and territory switching may 2010, Gómez et al. 2010, Claramunt et al. exert more cryptic forms of sexual selection 2011). (Morton et al. 2000, Tobias et al. 2009a). These factors help to explain why the These features contrast with many avian output of research focused on suboscines has model systems, which tend to have short-term increased exponentially in recent years (Fig. 1). pair-bonds, seasonal territoriality and high- The goal of this symposium was to summarise levels of overt sexual selection, particularly advances in our understanding of suboscine in the temperate zone. Even tropical studies birds, to emphasise the insights they provide often focus on visually attractive species with on life-history evolution, signal evolution and extreme sexual dichromatism and male-biased speciation, and to clarify the main avenues for ornamentation, such as manakins (Pipridae). future research. Thus, tracheophone suboscines offer useful insight into overlooked questions about WHAT DO SUBOSCINES TELL US the origins and implications of long-term ABOUT AVIAN LIFE HISTORIES? monogamous partnerships and selection on females (Tobias et al. 2012a). Much of the -HII  %UDZQ VXPPDUL]HG VRPH ÀQGLQJV RI  work to date has focused on the evolution of long-term population studies of understory communal displays, such as duets, and their species in the lowland forests of central multiple functions in cooperative resource Panama. These studies include capture-mark- defense, mate defense (Seddon & Tobias 2006) release (CMR) sampling that was initiated in DQGVH[XDOFRQÁLFWEHWZHHQSDUWQHUV 7RELDV  1979 and continues today, along with a series Seddon 2009c). of single species or comparative studies often 7ZR ÀQDO UHDVRQV ZK\ WUDFKHRSKRQH involving species from tropical and north suboscines are becoming increasingly popular temperate latitudes. Suboscine passerines are in studies of evolution and ecology are their prominent in the sample, e.g. 25 (71%) of 35 enigmatic evolutionary history and sheer VSHFLHVIRUZKLFKGDWDDUHVXIÀFLHQWWRHVWLPDWH diversity. Because their plumage is relatively demographic parameters. Others studies subdued, they have proved to be a hotbed for conducted in neotropical forests report similar the discovery or description of cryptic species proportions of subocines when sampling (e.g. Zimmer 1997, Isler et al. 2007, 2009, Chaves understory species with mist nets (see Karr et et al. 2010) and genera (Chesser et al. 2009, al 1990). Claramunt et al., 2010, Derryberry et al., 2010a, A series of analyses comparing tropical and 2010b). Moreover, the challenge of numerous north temperate species indicates a complex unresolved evolutionary relationships has suite of associations among key traits such attracted the attention of molecular biologists, as survival rate, body mass, stress responses, such that extensive phylogenetic trees are now reproductive effort, energetics, and immune available (e.g. Irestedt et al. 2002, Chesser 2004, function (see summary in Robinson et al. Moyle et al. 2009, Derryberry et al. 2011). 2010). The "fast-slow" axis summarizing the This combination of high species richness pace of life histories is a useful metaphor for and availability of phylogenetic data has made comparative studies, but tropical and temperate the tracheophone suboscines an increasingly species do not necessarily ordinate "cleanly" on important system for multi-species studies this gradient. Comparison of species sampled testing evolutionary and ecological theory, and in North America and Panama indicate that for PRGHOV RI GLYHUVLÀFDWLRQ LQ SDUWLFXODU HJ certain traits such as energy expenditure (e.g.,

264 THE IMPORTANCE OF NEOTROPICAL SUBOSCINE BIRDS AS STUDY SYSTEMS IN ECOLOGY AND EVOLUTION

ÀHOGPHWDEROLFUDWH DQGFRQVWLWXWLYHLPPXQH of evolution. Oscine song has been used to function (i.e., the part of immune system that test numerous evolutionary ideas, but the is not induced by the presence of a pathogen), fact that in many species these songs develop tropical species do seem to have a slow pace through an imprinting-like process means that of life whereby investment is structured conclusions may not be valid. For example, it is by a comparatively long expected lifespan. often argued that habitat-related differences in Alternatively, parental effort and survival rate oscine song are the result of acoustic adaptation do not exhibit an obvious tradeoff. The classic (e.g. Nicholls et al. 2006, Derryberry 2009) but view of avian life histories at tropical latitudes it could just as easily be explained by young is that they live longer and therefore invest less individuals learning the songs, or parts of in any one reproductive cycle. songs, that they perceive most clearly in their The characteristically small clutch size of natal habitat (Hansen 1979). For this reason, tropical species is typically invoked as evidence habitat-associated patterns of oscine song of this tradeoff. Yet, a series of recent studies YDULDWLRQ PD\ ODFN D JHQHWLF EDVLV UHÁHFWLQJ conducted on the Western Slaty Antshrike phenotypic plasticity rather than acoustic (Thamnophilus atrinucha  UHSRUWV VLJQLÀFDQW adaptation (Ripmeester et al. 2010). Similarly, LQYHVWPHQW ZLWK UHVSHFW WR SRVWÁHGJLQJ oscine song convergence in contact zones parental care (Tarwater & Brawn 2010). has been attributed to convergent character Tropical species may therefore have a “quality displacement (Cody 1969) but it could simply over quantity” strategy that is somewhat EHH[SODLQHGE\KHWHURVSHFLÀFFRS\LQJZKHUH independent of expected longevity. one species accidentally learns the song, or Overall, these studies reveal little “signal” or song types, of another species (Helb et al. constraint owing to phylogenetic history (e.g., K. 1985). Again, the convergent songs produced Lee unpublished MS). Nonetheless, Cohen et by this form of copying lack a genetic basis, al. (2008) report that correlations among traits and therefore do not qualify as character (e.g., between concentrations of circulating displacement driven by divergent selection antioxidants and survival rate), and therefore (Tobias & Seddon 2009b). potential tradeoffs, can vary between suites of Because of these issues, the nature of oscine and suboscines. It may be that certain song development in suboscine birds takes traits are somewhat constrained by history while on greater importance. Suboscine songs are others vary more “freely” within a clade. Clearly, often proposed to develop without learning much of what we know about the demography (Kroodsma 1984, Isler et al. 1998, Zimmer and life histories of tropical species comes from & Isler 2003), potentially offering a useful studies of suboscines. The message emerging contrasting system for studies of signal from these studies is that the life histories of evolution. However, this paradigm has been tropical species are not easily categorized and that challenged over recent years, suggesting further studies are required in diverse ecological that further work is required to validate settings within the Neotropics. assumptions. To address this question, Spotted Antbirds (Hylophylax naevioides) were reared by DEVELOPMENT, FUNCTION hand from the egg in soundproofed aviaries at AND EVOLUTION OF SONG IN the Smithsonian Tropical Research Institute in NEOTROPICAL SUBOSCINES Panama. Developing chicks were raised either in silence or were exclusively exposed to the song Nathalie Seddon discussed the implications of a related species with a distinctly different of song learning, or lack thereof, for studies song (Hylophylax naevius  $OO RI  WKH ÀYH

265 TOBIAS ET AL. individuals that survived to maturity produced (3) in one species (Thamnophilus doliatus), captive normal adult song, which is consistent with individuals produced normal songs as adults the hypothesis that tracheophone suboscines after being reared in silence or exposed to develop songs without learning. KHWHURVSHFLÀFWXWRUVGXULQJWKHQHVWOLQJSKDVH ,QWKHOLJKWRIWKHVHÀQGLQJVLWLVXVHIXOWR (Kroodsma 1984); (4) unlike hybrid oscines weigh up the evidence that song learning may be in which songs are typically copied from the widespread in suboscines. Looking broadly across parental male, hybrid tracheophone suboscines all suboscine species, rudimentary song learning produce structurally intermediate songs has been suspected in only three species, all of (Cadena et al. 2007). We also note that there are which have lekking or polygamous reproductive no cases of lekking or polygamous reproductive strategies. Trainer et al. (2001) proposed that strategies in this clade (Marantz et al. 2003; male Chiroxiphia linearis adjust song frequency Remsen 2003; Zimmer & Isler 2003). These by copying lek-mates, yet Trainer & Parsons facts, in conjunction with the evidence from (2002) found no microgeographic variation captive-rearing experiments, are consistent with in song structure, suggesting that learning is the idea that song learning is minimal, or even PLQRU RU DEVHQW 6LPLODUO\ OHNVSHFLÀFLW\ RI  nonexistent, in all tracheophone suboscines. songs in Lipaugus vociferans may indicate learning Minimal learning in suboscines adds weight (Fitzsimmons et al. 2008), but the evidence is to recent studies showing that acoustic structure ZHDN .URRGVPD )LQDOO\WKHÀQGLQJWKDW of suboscine songs is predicted by sound geographic variation in male songs of Procnias transmission properties of Amazonian habitats, tricarunculata was not explained by genetic variation and therefore subject to diversifying selection is again suggestive of learning (Saranathan et in heterogeneous environments (Tobias et al. 2007), as this tends to produce a mismatch al. 2010). It also helps to explain high levels between vocal and genetic variation (Nicholls et of stereotypy and individual distinctiveness, al. 2006). However, the subtle mismatch detected features which have been shown to facilitate in Procnias tricarunculata could potentially be individual (mate) and species recognition in explained by phenotypic plasticity unrelated to antbirds, even when overall differences in signal learning. Thus, the evidence for song learning in design are very small (Seddon & Tobias 2010). suboscines remains weak, and entirely restricted 7KHVHÀQGLQJVÀWZLWKWKHUHVXOWVRIRWKHUPDWH to lineages with lek-breeding reproductive removal and playback experiments in Amazonia strategies (i.e. strong sexual selection). FRQÀUPLQJ WKDW PDOH DQG IHPDOH VRQJV LQ Balanced against these largely inconclusive antbirds have dual functions in mate attraction cases, we note that experimental studies in and territory defense (Tobias et al. 2011). Taken socially monogamous non-tracheophones WRJHWKHU WKHVH ÀQGLQJV VXJJHVW WKDW VRQJ found no evidence of learning (Kroodsma 1984), divergence, mediated by ecological adaptation nor the forebrain cell clusters that control song and social selection, could play a key role in the acquisition in oscines (Kroodsma and Konishi GLYHUVLÀFDWLRQRI VXERVFLQHELUGV 1981). Switching attention to tracheophone suboscines, several studies suggest that their USING SONG RECORDINGS AND songs are innate: (1) individual variation in song 3/$<%$&.(;3(5,0(176720$3 structure is low, with no indication of mimicry, TERRITORIES AND INFER SONG repertoires and dialects (Lindell 1998; Bard et al. FUNCTION 2002; Seddon & Tobias 2006); (2) geographical variation in songs and genes is typically The simplicity and stereotypy of suboscine concordant (Isler et al. 2005; Chavez et al. 2010); songs suggests that they are amenable to

266 THE IMPORTANCE OF NEOTROPICAL SUBOSCINE BIRDS AS STUDY SYSTEMS IN ECOLOGY AND EVOLUTION automated song feature extraction procedures convergence among the sexes might facilitate used to identify songs to species (Trifa et al. 2008), intersexual competition in ground antbirds. or even individuals (Bard et al. 2002, Kirschel et al. 2009, 2011), with potential applications to MORPHOLOGICAL ADAPTATION improving our understanding of the ecology SHAPES VOCAL EVOLUTION IN of poorly known species. Early attempts A MORPHOLOGICALLY DIVERSE to apply automated algorithms to the vocal RADIATION OF SUBOSCINE BIRDS LGHQWLÀFDWLRQRIDQWELUGVSHFLHVRFFXUULQJLQ a Mexican rainforest worked reasonably well, Divergence of signals used in mate choice ZLWK  VXFFHVVIXO FODVVLÀFDWLRQ DFKLHYHG and male-male competition can promote the (Trifa et al. 2008). Alex Kirschel presented work process of speciation (Coyne & Orr, 2004). exploring this further at the individual level in Thus, understanding the evolutionary forces the Mexican Antthrush (Formicarius moniliger), that shape signal divergence is fundamental a monomorphic species where female song to our understanding of phenotypic evolution appears indistinguishable from male song. DQG GLYHUVLÀFDWLRQ 2QH LPSRUWDQW URXWH RI  Like many ground antbirds (), signal divergence is via ecological selection 0H[LFDQ DQWWKUXVK DUH YHU\ GLIÀFXOW WR VHH LQ on traits related to signal production. There WKH ÀHOG VR LGHQWLI\LQJ LQGLYLGXDOV RU WKHLU are often biomechanical limitations on the sex is very challenging. Using song recordings production of signals, such as limits on DQG VWDWLVWLFDO FODVVLÀFDWLRQV KRZHYHU LW ZDV movements of the vocal tract during song possible to identify over 30 individuals in a 50 production in birds (Nowicki et al. 1992). hectare study area in Chiapas, Mexico, and to Signals may therefore diverge as a by-product map territory occupancy over a 5-year period. of morphological adaptation to different Songs were found to be largely invariant from foraging niches and habitats (Podos & Hendry, year to year and individuals’ songs could thus 2006). Such morphological traits have been be recognized with accuracies over 80% referred to as ‘magic traits’ (Gavrielts 2004) among different years. Territory locations when they affect the production of mating ZHUHGHWHUPLQHGE\PDSSLQJZKHUHLGHQWLÀHG signals because divergent ecological selection birds were recorded singing, including where can give rise indirectly to non-random mating. possible, with the use of a wireless sensor Much of the evidence for an indirect effect network (Collier et al. 2010, Kirschel et al. of ecological selection on signals comes from 2011). Based on the distribution of songs it was studies of oscine song (Badyaev et al. 2008, possible to determine that shapes and sizes of Ballentine, 2006; Huber & Podos, 2006; Podos, territories can vary over time when individuals 2001). The link between ecological selection are replaced from their territories, and territory and signal evolution is particularly clear in birds dynamics varied between males and females (Podos, 2001), as the organ used to forage, (Kirschel et al. 2011). Moreover, by identifying the beak, can also be used to modulate the the song of each individual, it was possible to resonance properties of the vocal tract during determine when males and females sang. The sound production (Westneat et al. 1993). For song similarity between the sexes – a method to H[DPSOHEHDNVL]HDQGVKDSHLQ'DUZLQ VÀQFKHV distinguish song to sex has still not been found is often forwarded as one of the best examples – suggests convergence between the sexes in of a 'magic trait' linking ecological divergence territory defense. Intrasexual territory defense to reproductive isolation (Pfennig & Pfennig, appears commonplace in suboscines (Seddon 2010; Servedio et al. 2011). Because most work & Tobias 2006, Tobias et al. 2011), but song on the indirect effects of ecological selection

267 TOBIAS ET AL.

KDYH EHHQ FRQGXFWHG RQ RVFLQHV LW LV GLIÀFXOW we predicted a negative relationship between WRWHDVHDSDUWWKHLQÁXHQFHRIFXOWXUDOSURFHVVHV beak size and ability to perform the trade-off on vocal evolution from the potential impact between frequency bandwidth and pace. of morphological and ecological adaptation Our results suggest that the proximate (Seddon, 2005), and suggests that the conclusions IHDWXUHV RI  VLJQDO SURGXFWLRQ LQÁXHQFH WKH of previous studies may only apply to song- HYROXWLRQ DQG GLYHUVLÀFDWLRQ RI ZRRGFUHHSHU learning birds (ϳ 40% of all avian species). A few songs (Derryberry et al. 2012). We found studies outside of oscines (Anatidae: Hausberger HYLGHQFHWKDWZRRGFUHHSHUVRQJVKDYHGLYHUVLÀHG et al. 1991; Furnariidae: Palacios & Tubaro, 2000; within a bounded acoustic space such that slow Thamnophilidae: Seddon, 2005) suggest that the songs are produced at a range of frequency mechanistic link between beaks and songs may bandwidths but as song pace increases, maximal be more widespread but its generality remains values of frequency bandwidth decrease. We unclear. Here, we explore the interface between also found a positive relationship between beak morphological and vocal evolution in a major size and ability to perform the trade-off between radiation of suboscine birds, the woodcreepers frequency bandwidth and pace: species with (Dendrocolaptinae). Unlike oscine passerines large beaks tend to produce low performance (the focus of previous studies), suboscines make songs, whereas species with small beaks tend to ideal subjects because they develop their songs produce high performance songs. The evolution with minimal learning, and hence patterns of of performance is associated closely with the vocal divergence are not complicated by cultural evolution of beak size over time. Altogether, evolution. RXUÀQGLQJVVXJJHVWWKDWOLPLWDWLRQVRQVLJQDO Using a well-resolved molecular phylogeny production may play an important role not only of the woodcreepers (Derryberry et al., in the evolution of oscine songs but also in the 2011), we tested the vocal tract constraint evolution of vocal signals in woodcreepers. Our hypothesis (Podos, 1997). This taxonomically results add weight to previous studies proposing widespread constraint is a tradeoff between a link between beak size and song structure in the rate at which sounds are produced and suboscines (Palacios and Tubaro, 2000, Seddon, the frequency bandwidth of those sounds, as 2005), suggesting that correlated evolution via described in more than 40 species of oscines biomechanical constraints may be widespread (Passeri; reviewed in Podos et al., 2009) in birds. including a large number of wood warblers Because divergence in woodcreeper vocal (Parulidae: Cardoso and Hu, 2011) and one signals is in part a by-product of ecological species of seabird (Stercorariidae: Janicke et selection on beak morphology, our results al. 2008). If this constraint is an important have important implications for the role IDFWRULQVRQJGLYHUVLÀFDWLRQDQGHYROXWLRQLQ RI  HFRORJ\ LQ VXERVFLQH GLYHUVLÀFDWLRQ :H suboscines, then woodcreeper songs should hypothesize that strong ecological selection occupy a bounded acoustic space of frequency during the adaptation of woodcreepers bandwidth as a function of the rate of note to different habitats and foraging niches production. We also tested the hypothesis that promotes divergence in beak morphology there is a biomechanical limit on performance among species, and that this leads, indirectly, of this motor constraint related to beak size to acoustic divergence in songs. Because (Podos, 2001). This hypothesis has been vocalizations mediate species recognition in H[DPLQHGPRVWLQWHQVLYHO\LQ'DUZLQ·VÀQFKHV this clade, our results are also consistent with (Herrel, et al. 2008; Huber and Podos, 2006; the idea that beak morphology serves as a 3RGRV   $V IRXQG LQ 'DUZLQ V ÀQFKHV ‘magic trait’ not only in some oscine clades but

268 THE IMPORTANCE OF NEOTROPICAL SUBOSCINE BIRDS AS STUDY SYSTEMS IN ECOLOGY AND EVOLUTION across the entire passerine radiation (>5000 VHYHUDOROGIXUQDULLGOLQHDJHVZLWKLQWHUVSHFLÀF species), and that ‘magic traits’ themselves are territoriality coexist with remarkably similar relatively widespread (Servedio et al. 2011). songs, raising the possibility that character Nonetheless, we still have much to learn about convergence has been driven by competitive the extent to which ecological selection on LQWHUDFWLRQV 7KLV ÀWV ZLWK HYLGHQFH IURP beak morphology has had a pleiotropic effect Hypocnemis antbirds that competing species RQWKHGLYHUVLÀFDWLRQRI VRQJDQGWKHH[WHQW use convergent male songs to defend WR ZKLFK VRQJ GLYHUJHQFH LQ WXUQ LQÁXHQFHV WHUULWRULHV DJDLQVW KHWHURVSHFLÀFV 7RELDV  reproductive isolation in suboscine clades. Seddon 2009b). Moreover, even though such songs also function in mate attraction (Tobias THE ROLE OF SPECIES et al. 2011), their convergent design does INTERACTIONS IN PHENOTYPIC not lead to hybridization because females EVOLUTION are adept at discriminating between species and even individuals on the basis of subtly Classical evolutionary theory predicts that different vocalisations (Seddon & Tobias phenotypes of closely related species diverge 2010). These lines of evidence suggest that in sympatry by character displacement, divergent character displacement may apply i.e. selection acting to minimize costs of to the recognition mechanism rather than to ecological and reproductive interference the acoustic trait itself. (Grant 1972, Losos 2000, Pfennig & Pfennig 2009). However, direct evidence Future steps of divergent character displacement is Genetics underlying song design. largely restricted to young taxa, and much Fleshing out the genetic sampling required remains to be learnt about how species at the species level, particularly across tyrant- interactions shape phenotypic evolution Á\FDWFKHUVHWF over the longer timeframes of evolutionary True impression of biological diversity which radiations. Joe Tobias reported an extensive seems to be greatly underestimated. comparative analysis designed to explore Further exploration of use of song in this question, using Neotropical ovenbirds DXWRPDWHG LGHQWLÀFDWLRQ RI  VSHFLHV DQG as model systems. Data on ecological traits individuals. (beak shape and tarsus length) and signaling traits (song structure) were collected from Studies should be very cautious pooling VSHFLPHQV DQG ÀHOG UHFRUGLQJV RI  samples of oscine and suboscine species OLQHDJHV LQFOXGLQJ LQWUDVSHFLÀF OLQHDJHV  together. The results showed that occurrence in sympatry did not predict trait divergence, These factors make many suboscines ideal for contrary to the predictions of character ÀHOGVWXGLHVRI EHKDYLRUDQGOLIHKLVWRU\DQG GLVSODFHPHQW WKHRU\ 7KH RQO\ VLJQLÀFDQW for testing broader hypotheses about the role pattern detected was greater similarity of of social and ecological selection on evolution songs in sympatric lineages versus allopatric DQGGLYHUVLÀFDWLRQ lineages. This apparent convergence in songs can either be attributed to acoustic adaptation ACKNOWLEDGEMENTS to shared environments, or to convergent FKDUDFWHUGLVSODFHPHQWGULYHQE\LQWHUVSHFLÀF :H WKDQN WKH 12& VFLHQWLÀF SURJUDP territoriality (Cody 1969). It was noted that committee for their efforts in organizing an

269 TOBIAS ET AL. excellent meeting. We also thank numerous (rather than elaborate) sexual signals. Am Nat people who contributed to research presented 178: 679–686. in this symposium, including Adam Baker, Chaves, J. C., A. M. Cuervo, M. J. Miller, C. D. Santiago Claramunt, Martin Cody, Travis Cadena, (2010) Revising species limits in a Collier, Zachary Harlow, Robert Ricklefs, group of Myrmeciza antbirds reveals a cryptic Charles Taylor, Janeene Touchton, Edgar species within M. laemosticta (Thamnophilidae). 9DOOHMR:HDUHDOVRJUDWHIXOWRQXPHURXVÀHOG Condor 112: 718. ornithologists, collectors and institutions for Chesser R. T. (2004). Molecular systematics of New providing vocalizations, specimens and tissues World suboscine birds. Mol Phylogenet Evol. used in these studies. 32: 11–24. Chesser R. T., Claramunt S., Derryberry E., & REFERENCES %UXPÀHOG57*HRFHUWKLDDQHZJHQXV of terrestrial (Aves: Passeriformes: Badyaev A. V., Young R. L., Oh K. P., Addison C., Furnariidae). Zootaxa 2213: 64–68. 2008. Evolution on a local scale: Developmental, Claramunt, S. 2010 Discovering exceptional functional, and genetic bases of divergence GLYHUVLÀFDWLRQVDWFRQWLQHQWDOVFDOHVWKHFDVHRI  in bill form and associated changes in song the endemic families of Neotropical suboscine structure between adjacent habitats. Evolution passerines. Evolution 64: 2004–2019. 62: 1951–1964. Claramunt S., Derryberry E., Chesser R. T., Aleixo Ballentine B., 2006. Morphological adaptation $  %UXPÀHOG 5 7  3RO\SK\O\ RI  LQÁXHQFHV WKH HYROXWLRQ RI  D PDWLQJ VLJQDO Campylorhamphus, and description of a new Evolution 60: 1936–1944. for C. pucherani (Dendrocolaptinae). The %DUG6&0+DX0:LNHOVNL -&:LQJÀHOG Auk 127: 430–439. 2002. Vocal distinctiveness and response to Claramunt, S., E. P. Derryberry, J. V. Remsen, Jr., FRQVSHFLÀFSOD\EDFNLQWKH6SRWWHG$QWELUGD 57%UXPÀHOG+LJKGLVSHUVDODELOLW\ neotropical suboscine. Condor 104: 387. inhibits speciation in a continental radiation of %OHLZHLVV58OWUDYLROHWSOXPDJHUHÁHFWDQFH passerine birds. Proc. Roy. Soc. London B. distinguishes sibling bird species. Proc. Nat. Cody, M. L. 1969. Convergent characteristics in Acad. Sci. U.S.A., 1001: 16561–16564. V\PSDWULFVSHFLHVDSRVVLEOHUHODWLRQWRLQWHUVSHFLÀF %UXPÀHOG57-*7HOOR=$&KHYLURQ0' competition and aggression. Condor 71: 222–239. Carling, N. Crochet, & K. V. Rosenberg. 2007. Collier, T. C., Kirschel, A. N. G., & Taylor, C. E. Phylogenetic conservatism and antiquity of a 2010. Acoustic localization of antbirds in a tropical specialization: army--following in Mexican rainforest using a wireless sensor the typical antbirds (Thamnophilidae). Mol network. J. Aco. Soc. Am. 128: 182–189. Phylogenet Evol. 45: 1–13. Coyne J. A., & Orr H. A., 2004. Speciation. Cadena C. D., Lopez-Lanus B., Bates J. M., Krabbe Sunderland, MA: Sinauer Associates. N., Rice N. H., Stiles F. G., Palacio J. D. & Derryberry E, 2009. Ecology shapes birdsong 6DODPDQ3  $UDUHFDVHRI LQWHUVSHFLÀF evolution: variation in habitat and morphology hybridization in the tracheophone suboscines: explains variation in white-crowned sparrow Chestnut-naped Grallaria nuchalis x song. Am Nat 174: 24–33. Chestnut-crowned Antpitta * UXÀFDSLOOD in a Derryberry E., Claramunt S., Chesser R. T., Aleixo fragmented Andean landscape. Ibis, 149: 814– $&UDFUDIW-0R\OH5* %UXPÀHOG57 825. 2010a. Certhiasomus, a new genus of woodcreeper Cardoso G. C., & Hu Y., 2011. Birdsong (Aves: Passeriformes: Dendrocolaptidae). performance and the evolution of simple Zootaxa 2416: 44–50.

270 THE IMPORTANCE OF NEOTROPICAL SUBOSCINE BIRDS AS STUDY SYSTEMS IN ECOLOGY AND EVOLUTION

Derryberry E., Claramunt S., Derryberry G., disentangling the role of competition and habitat Chesser R. T., Cracraft J., Aleixo A., Pérez- ÀOWHULQJLQFRPPXQLW\DVVHPEO\RI1HRWURSLFDO (PiQ-5HPVHQ-U- %UXPÀHOG57 forest birds. J. An. Ecol. 79: 1181–1192. /LQHDJH GLYHUVLÀFDWLRQ DQG PRUSKRORJLFDO Grant, P. R. 1972. Convergent and divergent character evolution in a large-scale continental radiation: displacement. Biol. J. Linn. Soc. 4: 39–69. the Neotropical ovenbirds and woodcreepers Greenberg, R. & Gradwohl, J. 1983. Sex roles in the (Aves: Furnariidae). Evolution 65: 2973–2986. Dot-winged Antwren (Microrhopias quixensis), a Derryberry E., Claramunt S., O’Quin K. E., Aleixo tropical passerine. Auk 100: 920–925. $&KHVVHU575HPVHQ-9 %UXPÀHOG5 Greenberg, R. & Gradwohl, J. 1986. Stable territories T., 2010b. Pseudasthenes, a new genus of ovenbird and constant densities in tropical forest (Aves: Passeriformes: Furnariidae). Zootaxa 2416: insectivorous birds. Oecologia 69: 618–625. 61–68. Greenberg, R. & Gradwohl, J. 1997. Territoriality, Derryberry E. P., Seddon N., Claramunt S., Tobias adult survival, and dispersal in the Checker- -$%DNHU$$OHL[R$ %UXPÀHOG57 throated Antwren in Panama. J. Avian Biol. 28: (2012) Correlated evolution of beak morphol- 103–110. ogy and song in the Neotropical woodcreeper Hansen, P. 1979. Vocal learning: its role in adapting radiation. Evolution. In press. sound structures to longdistance propagation, Eaton, M. D. 2005. Human vision fails to and a hypothesis on its evolution. Anim. Behav. distinguish widespread sexual dichromatism 27: 1270–1271. among sexually “monochromatic” birds. Proc. Hausberger, M., Black, J. M., & Richard, J. P., 1991. Bill Nat. Acad. Sci. USA 102: 10942–10946. opening and sound spectrum in barnacle goose Eaton, M. D. 2006. A phylogenetic perspective on loud calls: individuals with ‘wide mouths’ have the evolution of chromatic ultraviolet plumage higher pitched voices. Anim Behav 42: 319–322. coloration in grackles and allies (Icteridae). Auk Helb, H.-W., F. Dowsett-Lemaire, H.-H. Bergmann, 123: 211–234. & K. Conrads. 1985. Mixed singing in European Fernandes, A. M., Wink, M., Aleixo, A. (2012) Mo- songbirds – a review. Z. Tierpsychol. 69: 27–41. lecular phylogeography of Chestnut-tailed Ant- Herrel, A., Podos, J., Vanhooydonck, B., & Hendry, bird (Myrmeciza hemimelaena FODULÀHVWKHUROHRI  A. P., 2008. Force-velocity trade-off in Darwin’s rivers in Amazonian biogeography. J. of Biog. Finch jaw function: a biomechanical basis for (in press). ecological speciation? Funct Ecol 23: 119–125. Fitzsimmons, L.P., Barker, N.K. & Mennill, D.J. Huber, S. K., & Podos J., 2006. Beak morphology (2008). Individual variation and lek-based vocal and song features covary in a population of distinctiveness in songs of the Screaming Piha Darwin’s Finches (Geospiza fortis). Biol J Linn (Lipaugus vociferans), a suboscine songbird. Auk, Soc 88: 489–498. 125: 908–914. Ippi, S., Vasquez, R. A., van Dongen, W. F. D. & Fleischer, R. C., Tarr, C., Morton, E. S., Derrickson, Lazzoni, I. (2011). Geographical variation in K. D. & Sangmeister, A. 1997. Mating system the vocalizations of the suboscine Thorn-tailed of the Dusky ( tyrannina), Rayadito Aphrastura spinicauda. Ibis, 153: 789–805. a tropical passerine, as assessed by DNA Irestedt, M., Fjeldsa, J., Johansson, U. S. & Ericson, ÀQJHUSULQWLQJ&RQGRU² P. G. P. (2002). Systematic relationships and Gavrilets, S. 2004. Fitness landscapes and the biogeography of the tracheophone suboscines origin of species. Princeton University Press, (Aves: Passeriformes). Mol Phylogenet Evol. 23: Princeton, NJ. 499–512. *yPH]-3*$%UDYR57%UXPÀHOG-*7HOOR Isler, M. L., Isler, P. R., & Whitney, B. M. (1998) & C. D. Cadena. 2010. A phylogenetic approach to Use of vocalizations to establish species limits

271 TOBIAS ET AL.

in antbirds (Passeriformes; Thamnophilidae). Lindell, C. (1998) Limited geographic variation in Auk 115: 577–590. the vocalizations of a neotropical furnariid, Isler, M. L., P. R. Isler, & B. M. Whitney. 2007. albescens. Wil. J. Ornith. 110: 368. Species limits in antbirds (Thamnophilidae): the Losos, J. B. (2000) Ecological character displacement Hypocnemis cantator complex. Auk 124: 11–28. and the study of adaptation. Proc. Natl. Acad. ,VOHU 0 / 35 ,VOHU  5 7 %UXPÀHOG  Sci. U.S.A., 97: 5693–5695 Clinal variation in vocalizations of an antbird Marantz, C., A. Aleixo, L. R. Bevier, & M. A. Patten, 7KDPQRSKLOLGDH DQGLPSOLFDWLRQVIRUGHÀQLQJ 2003. Family Dendrocolaptidae (woodcreepers). species limits. (Auk) 122: 433–444. Pp. 358–447 in The Handbook of the Birds of Isler, M. L., Isler, P. R., Whitney, B. M., Zimmer, K. J. the World, Vol. 8. Broadbills to (J. & Whittaker, A. 2009. Species limits in antbirds del Hoyo, A. Elliot, D. A. Christie, eds.). Lynx (Aves: Passeriformes: Thamnophilidae): an Edicions, Barcelona. evaluation of Frederickena unduligera (Undulated Morton, E.S. (1996) A comparison of vocal Antshrike) based on vocalizations. Zootaxa behavior among tropical and temperate 2305: 61–68. passerine birds. In: Ecology and Evolution Janicke T., Hahn S., Ritz M. S., & Peter H. U., 2008. of Acoustic Communication in Birds, (D.E. 9RFDOSHUIRUPDQFHUHÁHFWVLQGLYLGXDOTXDOLW\LQ Kroodsma & E.H. Miller, eds), Pp. 258–268. a nonpasserine. Anim Behav, 75: 91–98. Cornell University Press, Ithaca, New York. Karr, J. R., S. K. Robinson, R. O. Bierregaard, & Morton, E.S., Stutchbury, B.J.M. & Derrickson, J. G. Blake. 1990. Birds of four Neotropical K.C. 2000. Territory switching behavior in a forests. Pages 237–269 in Four Neotropical sedentary tropical passerine, the Rainforests, A. Gentry, editor. New Haven: Yale Cercomacra tyrannina. Behav. Ecol. 11: 648–653. University Press. 0R\OH5*57&KHVVHU57%UXPÀHOG-* Kirschel A. N. G., Cody M. L., Harlow Z. T., Tello, D. J. Marchese, and J. Cracraft. 2009. Promponas V. J., Vallejo E. E. & Taylor C. 3K\ORJHQ\ DQG SK\ORJHQHWLF FODVVLÀFDWLRQ RI  E. 2011. Territor ial dynamics of Mexican the antbirds, ovenbirds, woodcreepers, and allies Ant-thrushes Formicarius moniliger revealed by (Aves: Passeriformes: Infraorder Furnariides). individual recognition of their songs. Ibis 153: Cladistics 25: 1–20. 255–268. Nicholls, J. A., Austin, J. J., Moritz, C., Goldizen, A. Kirschel, A. N. G., Earl, D. A., Yao, Y., Escobar, I., W. ( 2 0 0 6 ) Genetic population structure and call Vilches, E., Vallejo, E. E., & Taylor, C. E. 2009. variation in a passerine bird, the Satin Bowerbird, Using songs to identify individual Mexican Ptilorhynchus violaceus. Evolution 60: 1279–1290. Antthrush (Formicarius moniliger): A comparison of Nowicki, S., Westneat, M. W., & Hoese, W., 1992. IRXUFODVVLÀFDWLRQPHWKRGV%LRDFRXVWLFV² Birdsong: Motor function and the evolution of Kroodsma, D. E. (1984) Songs of the Alder Flycatcher communication. Sem. Neur. 4: 385–390. (Empidonax alnorum) and Willow Flycatcher Palacios, M. G., & Tubaro, P. L., 2000. Does beak size (Empidonax traillii) are innate. Auk 101: 13–24. affect acoustic frequencies in woodcreepers? Kroodsma, D. E. (2011). Neither individually Condor 102: 553–560. distinctive songs nor “lek signatures” are Pfennig, K. S. & Pfennig, D. W. 2009. Character demonstrated in suboscine Screaming Pihas. displacement: ecological and reproductive Auk 128: 789–790. responses to a common evolutionary problem. Kroodsma D. E. & Konishi M. (1991). A suboscine Q. Rev. Biol. 84: 253–276. bird (Eastern Phoebe, Sayornis phoebe) develops Pfennig, D. W., & Pfennig, K. S., 2010. Character normal song without auditory feedback. Anim displacement and the origins of diversity. Am Behav 42: 477–487. Nat 176: S26–S44.

272 THE IMPORTANCE OF NEOTROPICAL SUBOSCINE BIRDS AS STUDY SYSTEMS IN ECOLOGY AND EVOLUTION

Podos, J., 1997. A performance constraint on the Seddon, N. (2005). Ecological adaptation and evolution of trilled vocalizations in a songbird species recognition drives vocal evolution in family (Passeriformes:Emberizidae). Evolution neotropical suboscine birds. Evolution 59: 200– 51: 537–551. 215. Podos, J., 2001. Correlated evolution of morphology Seddon, N., & Tobias, J. A. (2006) Duets defend DQGYRFDOVLJQDOVWUXFWXUHLQ'DUZLQ·VÀQFKHV mates in a suboscine passerine, the warbling Nature 409: 185–188. antbird (Hypocnemis cantator). Behavioral Ecology Podos, J., & Hendry, A. P., 2006. The biomechanics 17: 73. of ecologial speciation. In: Herrel A, Speck T, Seddon, N., & Tobias, J. A. (2007) Song divergence Rowe NP, editors. Ecology and biomechanics: a at the edge of Amazonia: an empirical test of mechanical approach to the ecology of the peripatric speciation model. Biological Jour- and plants: CRC Press, Boca Raton, FL. nal of the Linnean Society 90: 173–188. Podos, J., Lahti, D. C., & Moseley, D. L., 2009. Vocal Seddon, N., & Tobias, J. A. (2010) Character dis- performance and sensorimotor learning in placement from the receiver’s perspective: spe- songbirds. Adv Study Behav 40: 159–195. cies and mate-recognition despite convergent Remsen, J. V. 2003. Family Furnariidae (ovenbirds). signals in suboscine birds. Proceedings of the In: Handbook of the Birds of the World, vol. 8 (J. Royal Society B 277: 2475–2483. del hoyo, A. Elliot, D. A. Christie, eds), pp. Pp. Seddon, N., Merrill, R., & Tobias, J. A. (2008) Sexu- 162-357. Lynx Edicions, Barcelona. ally selected traits predict patterns of species Ricklefs, R. E., 2002. Splendid isolation: historical richness in a diverse clade of suboscine birds. ecology of the South American passerine fauna. American Naturalist 171: 620–631. J. Avian Biol. 33: 207–211. Seddon, N., Tobias, J. A., Eaton, M., & Ödeen, A. 5LFNOHIV5(  7KHXQLÀHGQHXWUDOWKHRU\RI  (2009) Human vision can provide a valid proxy biodiversity: Do the numbers add up? Ecology for avian perception of sexual dichromatism. 87: 1424–1431. Auk 127: 283–292. Ripmeester, E. A., J. S. Kok, J. C. van Rijssel, & H. Servedio, M. R., Doorn, G. S., Kopp, M., & Frame, Slabbekoorn. 2010. Habitat-related birdsong A.M., Nosil P. 2011. Magic traits in speciation: GLYHUJHQFHDPXOWLOHYHOVWXG\RQWKHLQÁXHQFH ‘magic’ but not rare? Trends Ecol Evol 26:389–397. of territory density and ambient noise in Tarwater, C. E., & J. D. Brawn. 2010. The post- European blackbirds. Behav. Ecol. Sociobiol. ÁHGJLQJ SHULRG LQ D WURSLFDO ELUG SDWWHUQV RI  64: 409–418. parental care and survival. Journal of Avian Robinson, W. D., M. Hau, K. C. Klasing, M. Wikelski, Biology 41: 479–487. J. D. Brawn., S. H. Austin, C. E. Tarwater, & R. E. Tarwater, C. E., R. E. Ricklefs, J. D. Maddox & J. 5LFNOHIV'LYHUVLÀFDWLRQRIOLIHKLVWRULHVLQ D. Brawn. 2011. Pre-reproductive survival in New World birds. Auk 127: 253–262. a tropical bird and its implications for avian life Lee, K. A., M. Wikelski, W. D. Robinson, T. R. histories. Ecology 92: 1271–1281. Robinson, & K. C. Klasing. 2008. Constitutive Tello, J. G., Moyle, R. G., Marchese, D. J. & immune defenses correlate with life-history Cracraft J. (2009). Phylogeny and phylogenetic variables in tropical birds. J. Anim. Ecol. 77: FODVVLÀFDWLRQRI WKHW\UDQWÁ\FDWFKHUVFRWLQJDV 356–363. manakins, and their allies (Aves: Tyrannides). Saranathan, V., Hamilton, D., Powell, G. V. N., Cladistics 25: 429–467. Kroodsma, D. E. & Prum, R. O. (2007). Tobias, J. A. & Seddon, N. (2009a) Sexual selec- Genetic evidence supports song learning in tion and ecological generalism are correlated in the Three-wattled Bellbird Procnias tricarunculata antbirds. Journal of Evolutionary Biology. 22: (Cotingidae). Mol Ecol 16: 3689–3702. 623–636.

273 TOBIAS ET AL.

Tobias, J. A. & Seddon, N. (2009b) Signal design and ecosystems: challenges and opportunities. perception in Hypocnemis antbirds: evidence for In Macdonald, D.W. and Willis, K. (eds): Key convergent evolution via social selection. Evo- Topics in Wildlife Conservation, Volume 2. Wiley, lution 63: 3169–3189. London. In press. Tobias, J. A. & Seddon, N. (2009c) Signal jamming Trainer, J. M., McDonald, D. B. & Learn, W. A. PHGLDWHVVH[XDOFRQÁLFWLQDGXHWWLQJELUG Cur- (2002). The development of coordinated rent Biology 19: 577–582. singing in cooperatively displaying long-tailed Tobias, J. A., Bates, J. M., Hackett, S. J., & Seddon, manakins. Behav Ecol 13: 65–69. N. (2008) Comment on: “The Latitudinal Gra- Trainer, J. M. & Parsons, R. J. (2001). Uniformity of dient in Recent Speciation and Extinction Rates long-tailed songs from three localities of Birds and Mammals.” Science 319: 901c. in Costa Rica. Wilson Bull 113: 431–434. 7RELDV-$$EHQ-%UXPÀHOG57'HUU\EHUU\ Trifa, V. M., Kirschel, A. N. G., Taylor, C. E., & E., Halfwerk, W., Slabbekoorn, & H., Seddon, Vallejo, E. 2008. Automated species recognition N. (2010a) Song divergence by sensory drive in of antbirds in a Mexican rainforest using Amazonian birds. Evolution 64: 2820–2839. Hidden Markov Models. Journal of the Tobias, J. A., Seddon, N., Spottiswoode, C. N., Acoustical Society of America 123: 2424–2431. Pilgrim, J. D., Fishpool, L. D. C., & Collar, Westneat, M. W., Long, J. H., Hoese, W., & Nowicki N. J. (2010b) Quantitative criteria for species S., 1993. Kinematics of birdsong—functional delimitation. Ibis 152: 724–746. correlation of cranial movements and acoustic Tobias, J. A., Gamarra-Toledo, V., Garcia-Olaechea, features in sparrows. J Exp Biol 182: 147–171. D., Pulgarin, P. C., & Seddon, N. (2011) Year- Woltmann, S., Sherry, T. W., & Kreiser, B. R. 2012. round resource defence and the evolution of A genetic approach to estimating natal dispersal male and female song in suboscine birds: social distances and self-recruitment in resident rain- armaments are mutual ornaments. Journal of forest birds. J. Avian Biol: 43: 33–42. Evolutionary Biology 24: 2118–2138. Zimmer, K. J. 1997. Species limits in Cranioleuca Tobias, J. A., Montgomerie, R., & Lyon, B. (2012a) vulpina. Ornithological Monographs 48: 849– The evolution of female ornaments and 864. weaponry: sexual selection, social selection and Zimmer, K. J. & Isler, M. L. 2003. Family ecological competition. Phil. Trans. Roy. Soc. B. Thamnophilidae (typical antbirds). In: Handbook In press. of the Birds of the World, vol. 8 (J. del hoyo, A. 7RELDV - $ úHNHUFLRøOX d +  9DUJDV ) Elliott & D. Christie, eds), pp. 448–681. Lynx H. (2012b) Bird conservation in tropical Edicions, Barcelona.

274