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Breeding Clusters in Birds: Ecological Selective Contexts, Mating Systems and the Role of Extrapair Fertilizations

Breeding Clusters in Birds: Ecological Selective Contexts, Mating Systems and the Role of Extrapair Fertilizations

SPECIAL ISSUE: BREEDING AGGREGATIONS

Animal Behaviour 143 (2018) 145e154

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Animal Behaviour

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Special Issue: Breeding Aggregations Breeding clusters in : ecological selective contexts, systems and the role of extrapair fertilizations

* Regina H. Macedo a, , Jeffrey Podos b, Jeff A. Graves c, Lilian T. Manica d a Departamento de Zoologia, Universidade de Brasília, DF, Brazil b Department of Biology, University of Massachusetts, Amherst, MA, U.S.A. c School of Biology, Harold Mitchell Building, University of St Andrews, St Andrews, Fife, U.K. d Departamento de Zoologia, Universidade Federal do Parana, Curitiba, PR, Brazil article info Sociality beyond mated pairs, whether in the form of nesting colonies, clustered territories or leks, fi Article history: presents an evolutionary puzzle because densely packed individuals typically incur high tness costs. Received 15 March 2017 One hypothesis to explain clustered distributions is that they overlie clumped distributions of resources. Initial acceptance 19 May 2017 However, numerous studies have shown that resource distributions are often insufficient to explain Final acceptance 11 December 2017 individuals' settlement decisions, suggesting that clustered breeding distributions are driven by other Available online 2 March 2018 types of benefits, possibly related to ecological, social and genetic factors. One can ask more specifically MS. number: SI-17-00239R whether cluster because of some underlying ecological factor, or whether aspects of their reproductive behaviour and mating systems are more influential. Accordingly, evaluating the influence of Keywords: upon the of mating systems can be crucial for understanding the underlying blue-black grassquit causes of animal aggregations. In this article, we review the behavioural of three types of mating clusters systems where breeding occurs in clusters: colonial, lekking and socially monogamous clustered terri- coloniality extrapair fertilization torial systems. We highlight sexual selection as a potential explanation for the emergence of aggrega- system tions in all three cases. In particular, we discuss the hidden lek hypothesis, which postulates that sexual selection aggregations in colonial and territorial can be driven by increased opportunities for extrapair social monogamy copulations. Finally, we feature our work with the blue-black grassquit, Volatinia jacarina, which illus- sociality trates the complexity of selective mechanisms that may favour territorial aggregations. © 2018 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Clustered breeding distributions have been described in very especially in light of the possible role of sexual selection and the diverse animal groups including , , fish, , di- importance of extrapair copulations. The term breeding clusters nosaurs, birds, and marine and terrestrial (Podulka, here refers to the nonrandom distribution of individuals across the 2004; Rypstra, 1985; Terhune & Brillant, 1996; Treves, 2000; landscape, such that they are close together in a pattern that does Varricchio et al., 2008). A core explanation for clustered distribu- not necessarily reflect resource distribution. We discuss clustered tions is that they reflect spatially uneven resource distributions, as breeding in three main contexts, coloniality, lekking and clustered many individuals in a population choose the same high-quality territoriality in socially monogamous species, for which we review sites (reviewed in Evans, Votier, & Dall, 2016). However, not all associated costs and benefits from an ecological context, while also clustered distributions can be explained by concentrated patches of exploring the possible impact of social and mating pressures. resources. Thus, a comprehensive understanding of breeding Finally, we consider how these factors might be playing out in a clusters requires looking beyond ecological resource distributions species we have featured in our own work, the blue-black grassquit, to other possible influences (Itzkowitz, 1978; Muller, 1998; Stamps, Volatinia jacarina. Most of our examples in this article are on birds, 1988). given our greater familiarity with this group, although we presume The primary goal of our article is to consider some open ques- that the conceptual context applies more generally to other animal tions about the evolution of nonresource-based breeding clusters, taxa. In many species that breed in clusters, individual territories are often small, tightly packed and very limited in resources. Aggre- * Correspondence: R. H. Macedo, Departamento de Zoologia, IB, Universidade de gated territorial breeding in these cases is known as colonial Brasilia, 70910-900, Brasília, DF, Brazil. breeding, and is taxonomically widespread (spiders: reviewed in E-mail address: [email protected] (R. H. Macedo). https://doi.org/10.1016/j.anbehav.2018.01.021 0003-3472/© 2018 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. SPECIAL ISSUE: BREEDING AGGREGATIONS

146 R. H. Macedo et al. / Animal Behaviour 143 (2018) 145e154

Whitehouse & Lubin, 2005; fish: Van Dongen, Wagner, Moodley, & necessarily correspond to their social choices (Reynolds, 1996). In Schaedelin, 2014; Schaedelin, van Dongen, & Wagner, 2015; birds: fact, conjectures about multiple mating among monogamous birds Varela, Danchin, & Wagner, 2007; reviewed in Wittenberger & began in the 1950s, based on observations of extrapair copulations Hunt, 1985; mammals: Pitcher, Harcourt, & Charrier, 2010; (EPCs; Bray, Kennelly, & Guarino, 1975; Fujioka & Yamagishi, 1981; Webber et al., 2016). A functional definition of coloniality is when Gladstone, 1979; von Haartman,1951). The discovery of widespread individuals aggregate in breeding densities well above that pre- EPCs suggested that postcopulatory, prezygotic selection might dicted by the distribution of resource patches (see Evans et al., have a greater impact on avian mating systems evolution than had 2016). previously been suspected. In birds, female multiple mating A second category of mating clusters not predicted by resource behaviour may trigger within the female distributions comprises lekking systems, wherein males usually reproductive tract, resulting in potential female control of paternity aggregate within small areas, called arenas, where they . (Birkhead & Møller, 1998). In general, however, very few Females visit and mate with clustered males, after which they studies have been able to test relationships between sexual selec- depart, build their nests and rear the offspring alone (Hoglund€ & tion, mating systems and sperm competition, and a clear under- Alatalo, 1995). In lekking systems, females choose partners based standing remains elusive. on male attributes only, without the influence of direct benefits such as territorial resources or potentially valuable paternal care. BREEDING AGGREGATIONS: ECOLOGICAL AND SEXUAL A third main context in which clustering is not directly predicted CORRELATES by resource distributions is in socially monogamous pairs whose territories contain resources other than breeding sites. Resource- Colonial Breeding Systems based territories are typically much larger than those found among colonial or lekking species. These types of nesting disper- Coloniality in birds has evolved independently at least 20 times sion patterns have been termed ‘neighbourhoods’ or ‘loose’ col- (Siegel-Causey & Kharitonov, 1990), suggesting that its benefits onies (Lack, 1968). Such clustering of all-purpose territories has not must be sufficient to override the inherent costs for individuals that been studied extensively, with most research to date having breed in colonies. Colonial breeding has multiple costs, such as the focused on birds (Almeida & Macedo, 2001; Bohorquez & Stiles, potential for increased transmission of pathogens and parasites, 2002; Greene, Muehter, & Davison, 2014; Tarof, Ratcliffe, elevated competition for resources including food and mates, and Kasumovic, & Boag, 2005; Tiainen, Vickholm, Pakkala, Piiroinen, higher mortality of young due to cannibalism and infanticide & Virolainen, 1983). Nevertheless, even in these systems, resource (Brown & Bomberger Brown, 1996; Møller, 1987). Some of the main distribution alone probably cannot fully explain the extent of driving forces for colonial nesting are ecological in . Absence clustering. In these cases, it has been proposed that sexual selection of specific predators, resource restriction and prey aggregation may mechanisms, such as the hidden lek models described below, could lead animals to establish colonies passively, where individuals do encourage the clustered patterns of territories within unsaturated not necessarily cooperate or even interact with conspecifics, but habitats of uniform quality. instead merely tolerate them. Theories describing animal breeding systems, and their di- A multispecies comparison based on observational data sug- versity across taxa, often build upon basic concepts of sexual se- gests that copulations with multiple partners occur more lection, since these may explain the variance often observed in frequently in colonial birds than in closely related solitary species reproductive success and reproductive skew (Andersson, 1994; (Møller & Birkhead, 1993; but see Griffith, Owens, & Thuman, Emlen & Oring, 1977; Owens & Bennet, 1997; Reynolds, 1996). 2002). Interestingly, the higher incidence of cuckoldry associated Sexual selection is a process favouring the exaggeration of sec- with clustered individuals can be considered both a cost, for ondary sexual traits that can increase an animal's chances of leaving cuckolded males (Alexander, 1974; Birkhead, 1979; Birkhead, Atkin, descendants in the next generation (Andersson, 1994; Darwin, & Møller, 1987; Gladstone, 1979), and a benefit, for females and 1871). According to this theory, individuals in better condition or males that achieve extrapair (Bain, Hall, & Mulder, 2014). bearing more extravagant ornaments should gain advantages in the The evolution of colonial nesting has been examined using two competition for sexual partners. Moreover, sexual selection should main approaches. One is the traditional ecological framework, be stronger in polygamous than in monogamous species, owing to a which entails a functional assessment of costs and benefits to group higher reproductive skew in the former, in which competition for living (Alexander, 1974; Wittenberger & Hunt, 1985). A second mates is more intense (Emlen & Oring, 1977). In polygamous sys- approach focuses on commodity selection, and builds on the tems, only a few individuals are able to attract multiple partners, assumption that individuals choose their breeding sites based upon thus increasing reproductive skew (Andersson, 1994). Multiple the availability of commodities such as habitat and mates. This mating behaviour should increase individual fitness when approach, which considers proximate mechanisms of habitat polygamy potential is high, that is, when mating partners or choice (Danchin & Wagner, 1997), posits that animals aggregate limiting resources are economically defensible, mostly when they incidentally because they make parallel choices regarding occur in clumped spatial distributions (Emlen & Oring, 1977). In preferred habitats. For example, in choosing a habitat, individuals contrast, social alliances between males and females in monogamy can copy the choices of other individuals that are breeding suc- tend to be maintained due to few opportunities for exclusive cessfully (Boulinier & Danchin, 1997; Danchin, Boulinier, & Massot, possession of multiple sexual partners, resulting in reduced vari- 1998). ance in reproductive success among males (Emlen & Oring, 1977; Considering first the traditional approach, the ecological bene- Owens & Bennet, 1997) and, in some cases, in females. fits that may favour the evolution of coloniality are numerous. A Historically, the classification of mating systems has relied upon geometrical model of proposes that coloniality may pro- the study of model species from temperate zones, and accordingly vide members with shorter distances to foraging areas (Horn, it has been difficult to account for unexpected behaviours in taxa 1968). Other possible benefits include high-quality but limited from less well-studied localities such as the tropics (Zuk, 2016; Zuk, nesting sites (Lack, 1968; Wittenberger & Hunt, 1985), protection Garcia-Gonzalez, Herberstein, & Simmons, 2014). The need for a from predators due to a location's inaccessibility (Buckley & better classification of animal mating systems was reinforced by the Buckley, 1980), decreased risks of due to the dilution discovery that the sexual mating behaviour of animals does not effect and increased opportunities for vigilance (Alexander, 1974; SPECIAL ISSUE: BREEDING AGGREGATIONS

R. H. Macedo et al. / Animal Behaviour 143 (2018) 145e154 147

Hamilton, 1971), alarm calling or mobbing under threat of preda- We believe that in the above-mentioned species, the tors (Charnov & Krebs, 1975). Indeed, studies have found that a benefits of coloniality probably outweigh costs associated with passive group size effect can dramatically increase survival and EPFs and that, in general, EPFs are not likely to be an important breeding success due simply to dilution, confusion and predator driver of coloniality, but rather a consequence of the high-density satiation effects (Barbosa, Moreno, Potti, & Merino, 1997; Hoogland nesting situation (see Westneat & Stewart, 2003). & Sherman, 1976). Applying the commodity selection approach requires investi- Lekking Breeding Systems gating how conspecifics can be used as cues to increase resource acquisition. One mechanism that could promote colonial nesting is A particularly fascinating form of breeding clusters occurs as the transfer of social information, initially termed the ‘information leks, wherein males aggregate only to obtain fertilizations, with centre hypothesis’ (Ward, 1965; Ward & Zahavi, 1973). Such infor- females being entirely responsible for postfertilization parental mation transfer could occur in key socioecological contexts, investment (Bradbury, 1981; Hoglund€ & Alatalo, 1995). Leks have providing cues about the location and quality of resources, preda- been documented in many taxa: insects, fish, anurans, possibly tors, and breeding and migration schedules. and newts, birds, and some mammals including The point we wish to emphasize here is that living in colonial and (Hoglund€ & Alatalo, 1995). In birds, lekking systems aggregations can also affect the dynamics of mating decisions, for have evolved in at least 14 independent cases across several fam- example by increasing opportunities for individuals to meet and ilies (e.g. Tetraonidae, Pipridae, Cotingidae, Paradisaeidae: interact. This can act as a positive selective pressure for greater Hoglund,€ 1989; Hoglund€ & Alatalo, 1995). Lekking systems provide densities of individuals, but might also increase competition for a unique opportunity for behavioural ecologists to document the mates. Draulans (1988) compared genera in the heron family causes and consequences of sexual selection, because mate selec- (Ardeidae) and found that colonial breeding is related to conspic- tion occurs independently of access to territorial resources or uous coloration and intensity of visual displays, which led him to paternal care, and female choice is thus based entirely upon male introduce what was then a new hypothesis. He suggested that traits and courtship displays. colonial breeding could generate greater chances of individuals In addition to the classical definition of leks (i.e. aggregations of meeting suitable partners, and thus increase sexual selection on displaying males), they can be further characterized by their mate competition. Because of increased competition in this social ecological contexts (Hoglund€ & Alatalo, 1995; Jiguet, Arroyo, & context, he also suggested that higher densities of individuals could Bretagnolle, 2000). ‘Aggregations on landmarks’ define leks that favour more elaborate visual displays during shorter periods. He occur where suitable display areas are limited, such as leks concluded that mate attraction could be a key selective pressure on hilltops or in sunspots within forest clearings (Alcock, 1983). leading to the evolution of coloniality for herons; we note that a Landmark lekking has also been identified for several , similar rationale has been applied to the evolution of leks including the white-winged , Eleothreptus candicans,in (Bradbury, 1981). Paraguay, in which males display along ridgelines in low savannah Mating interactions were initially regarded as diminishing the plateaus of scrubby vegetation (Pople, 2014). In ‘exploded leks’, advantages of coloniality, because males would suffer increased display territories are larger and more dispersed than in classical costs of cuckoldry through EPCs (Birkhead, Johnson, & Nettleship, leks. Examples include some birds of the Pipridae family, such as 1985; Emlen & Wrege, 1986; Møller, 1991). An alternative view, blue , caudata (Foster, 1981) and lance-tailed based upon studies of the purple martin, Progne subis, emphasized manakins, Chiroxiphia lanceolata (DuVal, 2007). Finally, ‘resource- that EPCs benefit some males and could favour colony formation in based leks’ occur when males aggregate near resources that are some contexts (Morton & Derrickson, 1990; Morton, Forman, & critical for females, as has been documented for some humming- Braun, 1990). These studies showed that young males lost pater- birds (Hoglund€ & Alatalo,1995; Stiles & ,1979). However, it can nity in their broods primarily to older males. Additionally, older be difficult to discriminate between resource-based lekking and males appeared to attract younger males to the colony, and resource defence nonlekking mating systems (sensu Emlen & frequently copulated with these males' mates. Female preferences Oring, 1977); this would require a close accounting of female for older males were further established in a later study, showing choice for males and resources as they relate to male territories (e.g. that younger males lost 43% of their paternity to EPCs, while older Alonso, Magana,~ & Alvarez-Martínez, 2012). males lost only 4% (Wagner, Schug, & Morton, 1996). In general, lekking species tend to experience parallel effects of One set of species with particular promise for assessing causal social interactions resulting from male aggregation and emanci- links between EPC frequency and the evolution of coloniality are pation from parental duties. Accordingly, in some lekking bird the , >95% of which are colonial (see Danchin & Wagner, systems, sexual selection appears to be very strong, generating a 1997). Fewer than 10% of seabird species have been examined to striking reproductive skew and high variance in male reproductive determine rates of extrapair fertilization (EPF); yet, of these, 41% success that favours a small subset of males within a given cluster (N ¼ 34) show a complete absence of extrapair paternity, compared (Hoglund€ & Alatalo, 1995; Mackenzie, Reynolds, Brown, & to 22% for other bird species. The absence of extrapair paternity in Sutherland, 1995; Wiley, 1991). However, in other species it ap- these species is particularly striking given the close physical prox- pears that females do not all converge in their choices of mates imity of mated pairs, and might be explained by these species' within and across leks, and that females thus mate with multiple longevity and high paternal investment (reviewed in Quillfeldt, males (see below for specific examples). Masello, & Segelbacher, 2012). One example of the first type, where there is concordance However, notable exceptions to this pattern have been found in among females in , concerns exploded leks of wire- other seabirds. Variation in mating strategies observed in some tailed manakins, Pipra filicauda, in which males gather in groups colonial species call attention to the possibility of high rates of EPC of two or more to perform coordinated displays to females. In a in colonial breeding systems. For instance, in the razorbill, Alca study of parentage, a single male in a lek sired 22 of 24 genotyped torda, a socially monogamous colonial seabird, males and females offspring (Ryder, Parker, Blake, & Loiselle, 2009). In this species, cluster in mating arenas for , but maintain other distinct territorial males sire 98% of offspring on average, to the virtual breeding territories for nesting (Wagner, 1992a, 1992b). Several exclusion of floaters, that is, nonterritorial young males that move other seabird species exhibit strikingly high rates of EPF (Table 1). freely between leks and participate in the coordinated displays SPECIAL ISSUE: BREEDING AGGREGATIONS

148 R. H. Macedo et al. / Animal Behaviour 143 (2018) 145e154

Table 1 Notable exceptions to monogamy in seabirds, as illustrated by high rates of extrapair fertilization (EPF)

Species % EPF Source

Broods Nestlings

Black-headed gull, Larus ridibundus 33 20 Lezalova-Pi alkov a, 2011 Thin-billed prion, Pachyptila belcheri e 21 Quillfeldt et al., 2012 Waved , Phoebastria irrorata 25; 14e21 25; 16.9 Huyvaert, Anderson, Jones, Duan, & Parker, 2000; Huyvaert, Anderson, & Parker, 2006 European shag, Phalacrocorax aristotelis 12.6 9.3 Graves et al., 1992, 1993 Cory's shearwater, Calonectris diomedea 11.6 11.6 Bried, Dubois, Jarne, Jouventin, & Santos, 2010 Adelie , Pygoscelis adeliae 11.1 9.1 Pilastro et al., 2001

(Ryder et al., 2009). Similarly, a large variance in reproductive noticed that a new arrival in springda first year birddwill try and success occurs in the black , Tetrao tetrix, in which approxi- try to establish a among a group of Song Sparrows, at the mately one-fifth of males in a lek gain all the copulations (Alatalo, same time ignoring equally favorable land at a little distance, that is Hoglund, Lundberg, & Sutherland, 1992). entirely unclaimed’. Other monogamous bird species in which Examples of the second type of lek where females mate with clustered territoriality has been described include willow warblers, multiple males include species that frequently have multiply sired Phylloscopus trochilus (Tiainen et al., 1983), lazuli buntings, Passer- broods, such as greater prairie chickens, Tympanuchus cupido (Hess, ina amoena (Greene et al., 2000, 2014), blue-black grassquits Dunn, & Whittingham, 2012), wild turkeys, Meleagris gallopavo (Almeida & Macedo, 2001) and least flycatchers, Empidonax mini- (Krakauer, 2008), sage grouse, Centrocercus urophasianus (Bird mus (Tarof et al., 2005). In dusky bush-tanagers, Chlorospingus et al., 2012) and some lekking species of waders (Lanctot, semifuscus, males defend clustered singing territories that are Scribner, Kempenaers, & Weatherhead, 1997; Lank et al., 2002; visited by females, but simultaneously defend other all-purpose Thuman & Griffith, 2005). In these species, the decreased skew in territories in which they conduct nesting activities (Bohorquez & male reproductive success presumably reduces the strength of Stiles, 2002). This is similar to the separation of mating and nest- sexual selection, and factors other than sexual selection probably ing sites in the razorbill (Wagner, 1992a, 1992b), mentioned play a strong role in driving clustered male distributions. previously. The severe reproductive skew identified in some species sug- In addition to the few mentioned above, there are many more gests that in at least some cases females are mostly concordant in territorial, socially monogamous species that breed in clusters, their mating choices, or at least that dominance hierarchies which leads us to ponder the selective pressures that might favour established among males predefine male breeding success (Beehler such clustering. One major category of selective pressures involves & Foster, 1988; Hoglund€ & Alatalo, 1995; McDonald, 2007; Ryder increased mating opportunities and reproductive gains, which in et al., 2009). However, current genetic analyses of paternity, as in socially monogamous species can be achieved through EPFs. This the studies cited above, are overturning this popular view relative hypothesis became plausible once EPFs were recognized as not only to lekking systems. a likely but also a frequent phenomenon, especially for socially Another intriguing feature of lekking systems is that mecha- monogamous birds (Birkhead & Møller, 1992). This resulted in nisms influencing female reproductive success have been difficult numerous studies attempting to explain the possible advantages to discern, as males do not provide food or other natural resources gained by females of these species. Studies that gathered obser- essential for female breeding (Bradbury, 1981; Hoglund€ & Alatalo, vational data indicated that male sexual behaviour resulting in EPC 1995). However, it is possible that multiple mating by females in was common, and that females seek extrapair partners as a stan- lekking systems (and in socially monogamous mating systems) dard matter of course (e.g. Graves, Hay, Scallan, & Rowe, 1992; benefits females directly by providing a safety measure against Kempenaers, Verheyen, & Dhondt, 1997; Stutchbury, 1998). As male infertility, thereby increasing female reproductive success noted above, new molecular tools allowed the comparative (Hasson & Stone, 2009; Morrow, Arnqvist, & Pitcher, 2002; Reding, assessment of extrapair paternity across different species, and 2015). These possibilities speak to the importance in these species showed that multiple paternity in various taxonomic groups occurs of direct benefits due to increased fertility effects, as well as indirect at moderate to high levels (reviews in Birkhead & Møller, 1998; (or genetic) benefits, and their weight in the evolution of female Griffith et al., 2002; Petrie & Kempenaers, 1998; Westneat & choice (Hoglund€ & Alatalo, 1995; Kokko, Brooks, Jennions, & Stewart, 2003). In some cases, molecular tools also verified that Morley, 2003). Regarding indirect benefits, females could achieve EPCs in some species did not always result in fertilizations (Gil, higher reproductive success by preferring sexual partners that are Slater, & Graves, 2007; Gyllensten, Jakobsson, & Temrin, 1990; more compatible with them, or that guarantee the transmission of Hunter, Burke, & Watts, 1992). good (Andersson, 1994) or attractive genes (Fisher, 1930)to The potential advantages females with social mates might gain their offspring. Dominant males that control display arenas are from multiple mating has been a topic of continuing interest. It is likely to be healthier than rival males, and should thus be preferred often suggested that multiple mating allows females to better as mates. Despite the suitability of bird lekking systems for testing ensure good genes' for their offspring, or ornamental traits that these hypotheses, our understanding of indirect benefits in the enhance future offspring attractiveness (reviews in Andersson, evolution of leks remains inadequate (Kempenaers, 2007; avian 1994; Jennions & Petrie, 2000; Johnstone, 1995; Mays & Hill, examples in Ekblom et al., 2004; Petrie, 1994; Sardell, Kempenaers, 2004; Westneat, Sherman, & Morton, 1990; Westneat & Stewart, & DuVal, 2014; examples in other groups: Brandt & Greenfield, 2003). Despite multiple models and theoretical interpretations, 2004; Hoglund€ & Alatalo, 1995; Jones, Quinnell, & Balmford, 1998). evidence of indirect fitness effects on sexual attractiveness remains relatively rare (but see Cator & Harrington, 2011; Ingleby et al., Socially Monogamous Territorial Systems 2013; Suzaki, Katsuki, Miyatake, & Okada, 2013; Taylor, Wedell, & Hosken, 2007; reviewed in Hettyey et al., 2009). Studies of some An early observation of clustered territories in birds described species have failed to find evidence for indirect fitness effects song sparrows, Melospiza melodia, and their preference for settling through good genes, as in a study of the coal tit, Periparus ater, near established territorial birds (Nice, 1937, page 73): ‘I have often where extrapair paternity rates were high but for which no SPECIAL ISSUE: BREEDING AGGREGATIONS

R. H. Macedo et al. / Animal Behaviour 143 (2018) 145e154 149 apparent long-term fitness benefits to females in extrapair matings hypothesis could apply when EPCs create similar conditions to were detected (Schmoll, Dietrich, Winkel, Epplen, & Lubjuhn, those observed in lekking species. One main prediction of the hy- 2002). A contrasting early example in field crickets, Gryllus bima- pothesis is that males cluster for the purpose of attracting females culatus, provided evidence for indirect fitness benefits, illustrating that are seeking EPCs. Another prediction is that, as in leks, females that male quality (defined as success in attracting mates) can be favouring certain males should result in skewed EPC distributions. heritable: males that had higher mating success produced sons that Accordingly, males with territories far from favoured males would obtained more copulations than did sons of less successful males have difficulty attracting a mate, and would do better by attempting (Wedell & Tregenza, 1999). In general, females that mate to defend a territory closer to one or more successful males. multiply may gain viability advantages for their offspring (see However, in contrast to lekking systems, socially monogamous Petrie, 1994; Welch, Semlitsch, & Gerhardt, 1998; reviewed in males also defend traditional territories (in territorial species) or Jennions & Petrie, 1997), greater assurance of genetic compatibility nests (in colonial species), and assist in caring for offspring pro- (reviewed in Akçay & Roughgarden, 2007 and Arct, Drobniak, & duced by their social mates. Thus, sexual selection and resulting Cichon, 2015) or increased offspring heterozygosity (Brown, 1997; EPCs might act as a driving force favouring clustered territories in Zeh & Zeh, 1996). Additionally, unlike in leks, females in social socially monogamous species. pairings that mate multiply may gain direct benefits such as new The hidden lek model coincides with two models hypothesized foraging opportunities, extra paternal care, potential future mate to underlie traditional leks. The hotshot model for leks suggests replacements (reviewed in Petrie & Kempenaers, 1998) and that females are attracted to and allow more copulations with increased fertilization success (Reding, 2015). specific males of a certain type (Beehler & Foster, 1988; Hoglund€ & In socially monogamous birds, a host of additional social and Robertson, 1990). In this context, females do not obtain specific ecological factors have been considered important in shaping advantages from male clustering, and could even suffer disadvan- extrapair mating behaviour; these include degrees of breeding tages from courtship disruptions. The second model is the female synchrony, migration patterns, rates of nest predation, habitat type preference model (Bradbury, 1981). According to this model, fe- and complexity, speed of pair formation, breeding density, adult males prefer clustered males because this allows them to draw male mortality and the need for male parental assistance (Biagolini, efficient comparisons of multiple male phenotypes, with solitary Westneat, & Francisco, 2017; Mays & Ritchison, 2004; males perhaps being ignored. In this case, females benefit from Spottiswoode & Møller, 2004; Stewart, Westneat, & Ritchison, male clustering by being able to evaluate larger numbers of in- 2010; Tryjanowski, Antczak, & Hromoda, 2007; Yuta & Koizumi, dividuals with greater efficiency. 2016; reviewed in Macedo, Karubiain, & Webster, 2008). One Despite the intuitive logical appeal of the hidden lek hypothesis, interesting angle in understanding the evolution of EPCs has been few empirical studies have applied the proposed models to to focus on specific male behaviours such as (1) those aimed at examine the underlying mechanisms that would favour clustered protecting paternity, for example mate guarding or frequent territoriality (Fletcher & Miller, 2006; Tarof et al., 2005). Evaluating copulation (reviewed in Harts, Booksmythe, & Jennions, 2016), and whether sexual selection mechanisms, in the form of hidden leks, (2) those intended to increase the chances of gaining access to fe- are responsible for the clustering of male territories requires males. In this latter category, we might regard the emergence of identifying appropriate species that exhibit specific traits, clustering as a mechanism for increasing male mating opportu- including: (1) the presence of territorial clumping in unsaturated nities, similar to what may also occur in colonies and leks, as habitats of relatively uniform quality; (2) the presence of pair bonds described above. and paternal care; (3) a lack of correspondence between ecological features and the distribution of territories; (4) the occurrence of THE HIDDEN LEK HYPOTHESIS: SEXUAL SELECTION AS AN EPC wherein females appear to select extrapair males; (5) an INTEGRATIVE EXPLANATION FOR BREEDING CLUSTERS absence of by extrapair males; and (6) a lack of resource monopolization by extrapair males (see Fletcher & Miller, The ‘hidden lek hypothesis’ (Wagner, 1993) synthesized ideas 2006; Wagner, 1993). Once these criteria are identified, other and observations that emerged from studies of extrapair paternity specific details become important, such as whether the distribution in colonial birds into a new logical framework, proposing that of EPFs is skewed, whether male attributes are associated consis- colony formation or territorial aggregations could be driven largely tently with successful siring of extrapair young, and whether by sexual selection. Roughly defined, a hidden lek is a cluster of higher densities of males are correlated with higher rates of EPC territorial, socially monogamous pairs that aggregate primarily due (i.e. whether the hotshot or female preference model is in effect). to the fitness advantages females gain through EPC (Danchin & Rarely have all these criteria been assessed for a single species, Wagner, 1997; Wagner, 1993, 1998). According to the hidden lek but attempts have been made with several species that exhibit hypothesis, the same mechanisms that favour the evolution of certain key criteria. For example, in the least flycatcher, although classical leks operate not just in polygamous species but also in several key predictions of the hidden lek hypothesis were upheld, socially monogamous, territorial species (Wagner, 1993). The one important prediction was not: a correlation between male formal hypothesis emerged from studies of the colonial system of centrality in clusters and their extrapair mating and siring success razorbills (Wagner, 1993). As mentioned previously, razorbills are a (Tarof et al., 2005). The bearded tit, Panurus biarmicus, is typically socially monogamous, biparental colonial seabird species in which loosely colonial and socially monogamous, but solitary nesting also females actively pursue EPCs, which occur in mating arenas set occurs. In colonies, females regularly solicit copulations from apart from the areas occupied by nests (Wagner, 1992a, 1992b, extrapair males (Hoi, 1997), and coloniality appears to be favoured 1992c). The mating arenas exhibit characteristics typical of leks: by female preferences to seek EPCs (Hoi & Hoi-Leitner, 1997). males cluster at these sites, and there are no resources available for Another species in which female mating tactics appear to favour females that visit the arenas. Additionally, extrapair males do not male aggregations is the black-capped chickadee, Poecile atrica- exhibit paternal care. Also in line with the lekking pattern was the pillus (Ramsay, Otter, & Ratcliffe, 1999). The hidden lek model has skewed distribution of EPC observed, with the two most successful also been extended recently to explain the high prevalence of EPFs males in a study obtaining 75% of all copulations (Wagner, 1992b). that occur in the cooperatively breeding superb fairy-wren, Malu- For socially monogamous, territorial species where both mem- rus cyaneus, which occupy year-round, all-purpose territories: bers of mated pairs invest in caring for offspring, the hidden lek ‘parasitic’, low-quality males aggregate near attractive, high-quality SPECIAL ISSUE: BREEDING AGGREGATIONS

150 R. H. Macedo et al. / Animal Behaviour 143 (2018) 145e154 males, and accordingly are able to secure approximately 33% of preferred males, because males with specific display traits extragroup fertilizations (Cockburn et al., 2009). By contrast, for the (including higher leaps) are found to be more successful in barn swallow, Hirundo rustica, a species that breeds either in soli- attracting mates (Carvalho et al., 2006; Manica et al., 2016). tary pairs or with groups of conspecifics, patterns of settlement are Available evidence suggests that a primary benefit of clustering not associated with observed differences in EPC rates exhibited by in these populations is facilitated access to material resources (Dias females (Safran, 2004, 2007). In this and other similar species, the et al., 2009). Comparative analyses of food availability and vege- hidden lek model cannot adequately describe the aggregation tation complexity in clusters versus solitary territories showed that patterns observed, and other explanations should be entertained. clumping of males was more common where grasses were taller In the long run, advancing our understanding of the hidden lek and producing more seeds, and where shrubs were abundant (Dias model, and its causes and consequences, will require identifying et al., 2009). Richer vegetation structure probably provides essen- additional candidate species for detailed study. tial resources for the survival and offspring provisioning of this granivorous bird during the breeding season, allowing males to BREEDING CLUSTERS IN THE BLUE-BLACK GRASSQUIT: HIDDEN avoid travelling long distances for foraging. Furthermore, the LEKS? greater density of shrubs in clusters is also advantageous for establishing and defending perches for attracting females for cop- A species of particular interest in the context of the hidden lek ulations, since displays are performed mostly on prominent hypothesis is the blue-black grassquit. This Neotropical grassland perches (Almeida & Macedo, 2001; Webber, 1985). Interestingly, is highly conspicuous during the breeding season, with birds in clusters may face a trade-off in displaying in terms of males clustering to display after arriving from migration (Almeida increased exposure to nest predators, compared to birds in solitary & Macedo, 2001). Courtship displays are complex and multi- territories. Nevertheless, males positioned in central territories modal, composed of repeated vertical flights termed ‘leap displays’. within clusters may offset this disadvantage, since predation rates At the vertical peak of each flight, males rotate forward and pro- are lower in central than in peripheral nests (Dias et al., 2009). An duce a buzzy vocalization that continues as they land (Manica, additional cost for males in clusters is that they usually engage in Graves, Podos, & Macedo, 2016). Males execute their leap displays more agonistic encounters with neighbours, which are potential repeatedly throughout the day, alternating with feeding, chasing rivals, than do males in solitary territories, suggesting that in- females and resting or singing on different perches. While dis- dividuals are involved in more intense social conflict when residing playing, males defend small all-purpose territories (13e72.5 m2, in clusters than when isolated (Dias et al., 2009). Thus, despite Almeida & Macedo, 2001) and engage in agonistic encounters with gaining easier access to food, more displaying sites and, possibly, intruding conspecific males (Webber, 1985). Aggregations of dis- more chances of attracting females, males still pay a price for playing males in open areas may reach up to 20 individuals, but it is breeding in aggregations. also possible to find individuals displaying solitarily (Dias, Evidence supporting the hidden lek pattern in blue-black Kuhlmann, Lourenço, & Macedo, 2009; Webber, 1985). At first grassquits has also emerged from studies of these birds' social glance, these clusters of displaying males and their behavioural and sexual behaviour. Breeding synchrony, measured as the per- repertoire resemble a lek (Murray, 1982; Webber, 1985). Accord- centage of fertile females per day, is notably higher in aggregations ingly, early descriptions of this species suggested that males were (28%) than among solitary territories (6%, Dias et al., 2009); this indistinguishable while singing in ‘chorus’ and displaying in ag- could facilitate EPCs by fertile females during extraterritorial forays gregations (Carvalho, 1957); the species was considered possibly within aggregations. Females might also prefer males already the only New World oscine to form lek-like breeding aggregations established in aggregations, as it allows them to better compare (Webber, 1985). However, closer examination revealed that males male phenotypes and obtain EPCs from preferred males (i.e. ‘female engaged in parental care and formed social bonds with females preference model of hidden lek’, Fletcher & Miller, 2006; this again (Alderton, 1963; Barnard, 1956), facts that precluded its classifica- reinforces the appearance of a lek-like in this spe- tion within a classical lek mating system (Hoglund€ & Alatalo, 1995). cies, Almeida & Macedo, 2001). None the less, the tight aggregations of blue-black grassquits with The occurrence of EPFs in blue-black grassquits is now well their conspicuous displays amount to what Webber (1985, page established; observed levels of EPFs range from moderate to high 545) described as ‘a richly-detailed avian oddity that ought to repay (63%, Carvalho et al., 2006;11e47%, Manica et al., 2016) and can further study’. vary substantially across years (Manica et al., 2016). Of various More than five decades after aggregations and displays in blue- display traits examined, leap display height seems to matter most black grassquits were first formally described, explanations for for females when choosing a social partner (Carvalho et al., 2006; their behaviour have been advancing through studies of ecological Manica et al., 2016). This trait is correlated with robust male and breeding parameters in central Brazilian populations (Aguilar, health (Aguilar, Maia, et al., 2008; Costa & Macedo, 2005; Manica Dias, Oliveira, & Macedo, 2008; Aguilar, Maia, Santos, & Macedo, et al., 2016) and is probably an important cue for females select- 2008; Almeida & Macedo, 2001; Dias et al., 2009; Manica et al., ing a high-quality future social father for their offspring. Mecha- 2016, 2017). Specific characteristics of the species make it a good nisms of female choice for engaging in EPCs, none the less, still lack model to tease out links between spatial distribution, resource a clear explanation. Chances of cuckoldry, or of any male gaining quality and the potential role of sexual selection. Notably, blue- EPFs, seem to be unrelated to any measured male display trait or to black grassquits fulfil at least three key assumptions of the hid- genetic compatibility with the female (Manica et al., 2016). One den lek hypothesis, outlined above (Fletcher & Miller, 2006; male visual signal that still needs to be explored is male Wagner, 1993, 1998). First, members of breeding pairs form a so- coloration. Evidence suggests that females could assess this signal cial alliance during each breeding attempt, with both members of when seeking prospective mates; notably, males with more blue- the pair executing parental duties. Second, tight male clustering black plumage (UV-shifted chroma) were seen to provide less creates a favourable scenario for females to seek copulations with food to their offspring (Diniz et al., 2015), a trade-off that might extrapair partners, which in turn are unlikely to provide paternal indicate greater emphasis on mating effort than on parental effort. care or access to limiting resources (Almeida & Macedo, 2001; Other male traits possibly shaped by female choice include be- Carvalho, Macedo, & Graves, 2006; Diniz, Ramos, & Macedo, haviours such as overall amount of time spent displaying (analo- 2015). Third, females can probably identify and select the same gous to lek attendance), and behavioural interactions with other SPECIAL ISSUE: BREEDING AGGREGATIONS

R. H. Macedo et al. / Animal Behaviour 143 (2018) 145e154 151 males within clusters (Castellano, 2009; Hill, 1991; Rintamaki,€ cluster, to the timing of territory acquisition, and to mating and Hoglund,€ Alatalo, & Lundberg, 2001). fertilization success. We also anticipate that cluster size will influ- In a recent study involving blue-black grassquits, we tested ence mating success, as a response to female preferences for whether the spatial and temporal distribution of males follows the maximizing chances of encountering larger numbers of potential hotshot model (Beehler & Foster, 1988) and/or the female prefer- extrapair partners. ence model (Bradbury, 1981), as described in the hidden lek hy- pothesis (Wagner, 1998). We monitored and sampled populations CONCLUSION across 3 years, and our genetic data allowed us to identify extrapair fathers and their offspring (Manica et al., 2016). Extrapair males Mating systems have traditionally been classified into discrete were either nesting elsewhere, settled within the same cluster categories, with socially monogamous and lekking mating systems where they gained extrapair fertilizations, or settled in a neigh- regarded as resulting from very different sets of selective pressures. bouring cluster (Manica, Graves, Podos & Macedo, n.d.; Fig. 1). We The hidden lek hypothesis adds a layer of complexity to the story, identified a variable clustering pattern: males settled into terri- by illustrating that the dividing lines between different mating tories either in large aggregations (up to 19 males) that extended systems can be blurry. Indeed, some mating systems, as we have over areas larger than 8000 m2, or in smaller groups of only two illustrated for the blue-black grassquit, have characteristics of both individuals. Across the 3 years, only two males established solitary lekking and nonlekking systems. It may be tempting to overlook territories. Males within clusters had different territorial estab- apparently uncharacteristic details and behaviours for the sake of lishment dates after arriving from migration, with intervals of up to simplicity. However, closer attention to variations across systems 84 days between the first and last male settling in the area. should reinforce the point that breeding systems can be complex Our assessment of the blue-black grassquit as a good candidate and that simplified explanations, although appealing, rarely cap- for the hidden lek scenario was based initially upon the evaluation ture reality with as much precision as we might hope. of the main criteria specified by the model. More precisely, the species exhibits territorial clumping in unsaturated habitats of relatively uniform quality; birds mate in social pairs and paternal Acknowledgments care is intense; the species has moderate to high rates of EPF; and extrapair males do not assist with parental care or monopolize any We acknowledge funding from Conselho Nacional de Desen- type of resource that females might require. Another more recent volvimento Científico e Tecnologico eCNPq (Grant No. 303664/ finding in line with the hidden lek hypothesis was that females 2014-2) for the fellowship to R.H.M. Logistic support was provided favour social mates with a specific display attribute, the consistent by University of Brasilia, University of Parana, University of Mas- execution of higher display leaps (Manica et al., 2016). However, sachusetts e Amherst and University of St Andrews. We also thank other predictions of the hidden lek model were not supported, such three referees for their suggestions, which helped to improve the as a positive association between male attributes and successful manuscript. siring of extrapair young. We are in the process of using the data collected across the 3 References years to test other aspects of the hidden lek hypothesis in more detail. Some other predictions we are testing are that leap display Aguilar, T. M., Dias, R. I., Oliveira, A. C., & Macedo, R. H. (2008). Nest-site selection by traits will correspond to the male's spatial position within the blue-black grassquit in a Neotropical savanna: Do choices influence nest suc- cess? Journal of Field , 79,24e31. Aguilar, T. M., Maia, R., Santos, E. S. A., & Macedo, R. H. (2008). Parasite levels in blue-black grassquits correlate with male displays but not female mate pref- erence. , 19, 292e301. Akçay, E., & Roughgarden, J. (2007). 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