Regina H. Macedo

Extrapair Paternity and Sexual Selection in Socially Monogamous Birds: Are Tropical Birds Different?

The Auk, Vol�� 125, Number 4, pages 769–777�� ISSN 0004-8038, electronic ISSN 1938-4254��  2008 by The American Ornithologists’ Union�� All rights reserved�� Please direct all requests for permission to photocopy or reproduce article content through the University of California Press’s Rights and Permissions website, http://www��ucpressjournals�� com/reprintInfo��asp�� �OI: 10��1525/au���2008��11008 Sexually elaborate traits, such as bright plumage and courtship signals, are generally thought to evolve through sexual selection (Andersson 1994), which requires variance in male mating success to operate (Arnold 1994)�� More than 90% of all birds are socially monogamous (Lac� 1968) and, therefore, are expected to exhibit low variance in mating success and wea� sexual selection; yet, paradoxically, many socially monogamous birds show the stamp of strong sexual selection in such traits as exaggerated plumage ornamentation and courtship displays�� Although �arwin (1871) suggested alternatives (Webster et al�� 2007), numerous recent genetic studies have suggested that extrapair paternity (EPP) may be the most li�ely resolution of this apparent paradox: if copulations outside of the pair bond are common, then variance in mating success may be far larger, and sexual selection much stronger, than suggested by social pairing success alone (Webster et al�� 1995)�� Indeed, <25% of birds studied to date are genetically monogamous (Griffith et al�� 2002), and studies have shown that EPP can generate strong sexual selection in socially monogamous systems (e��g��, Albrecht et al�� 2007, Webster et al�� 2007)�� However, despite two decades of wor�, we have only rudimentary understanding of the factors that lead to variation in EPP rates across populations (Griffith et al�� 2002, Westneat and Stewart 2003, Neudorf 2004)�� Conclusions regarding the role of EPP in sexual selection, however, must be ta�en with a large and important caveat, the so-called “temperate zone bias” (Stutchbury and Morton 2001): most studies have focused on temperate-zone birds, only a handful loo�ing at tropical species�� Given that most birds, by far, live and breed in the tropics, this omission is critical (see Martin 1996, 2004)�� Without a better understanding of the prevalence of factors contributing to EPP in tropical species, our ability to generalize about EPP and its role in sexual selection among socially monogamous species will remain limited�� �espite the widely recognized lac� of empirical data, tropical species are generally considered to have lower rates of EPP than temperate species�� For example, Stutchbury and Morton “Studies of temperate species

Coccidian oocyst parasitism in the blue-black grassquit: influence on secondary sex ornaments and body condition

Female choice for conspicuous secondary sexual traits, which often decrease male survival, is greatly debated in the sexual selection literature. The parasite-mediated sexual selection hypotheses suggest that parasite-resistant males should show greater expression of secondary sexual traits. Males in better condition should also have more extravagant ornamentation. According to these hypotheses, females that favour more conspicuous secondary sexual traits are choosing less parasitized males and/or those in better condition and should have offspring with better chances of surviving. We assessed interactions between the expression of secondary sexual traits, parasite load and body condition in the blue-black grassquit, Volatinia jacarina. We trapped and banded males and sampled intestinal parasites (coccidian oocysts). We considered plumage (percentage of blue-black coverage and coloration of feathers on rump and breast), display characteristics (frequency of events and height/frequency of leaps) and body condition (body mass and size, haematocrit and total plasma protein levels). There was a negative correlation between the number of oocysts and two secondary sexual traits, blue-black coverage and leap frequency. A negative correlation was also found between oocysts and two measures of body condition, body mass and size index. We found no correlation between body condition and secondary sexual traits. Results support parasite-mediated but not condition-dependent sexual selection. There were no correlations between body condition and secondary sexual traits, so parasites may affect secondary sexual traits directly.

Iridescent structural colour production in male blue-black grassquit feather barbules: the role of keratin and melanin

Iridescent coloration plays an important role in the visual communication system of many animal taxa. It is known that iridescent structural colours result from layers of materials with different refractive indexes, which in feathers usually are keratin, melanin and air. However, the role of these materials in the production of structural iridescent coloration is still poorly documented. Despite the great interspecific variation in the organization of such structures in bird plumage, melanin layers are usually considered too opaque, suggesting its main role is to delineate the outermost keratin layer and absorb incoherently scattered stray light. We combined spectrometry, electron microscopy and thin-film optical modelling to describe the UV-reflecting iridescent colour of feather barbules of male blue-black grassquits (Volatinia jacarina), characterized by a keratin layer overlying a single melanin layer. Our models indicate that both the keratin and the melanin layers are essential for production of the observed colour, influencing the coherent scattering of light. The melanin layer in some barbules may be thin enough to allow interaction with the underlying keratin; however, individuals usually have, on an average, the minimum number of granules that optimizes absorbance by this layer. Also, we show that altering optical properties of the materials resulted in better-fitting models relative to the empirically measured spectra. These results add to previous findings concerning the influence of melanin in single-layer iridescence, and stress the importance of considering natural variation when characterizing such photonic structures.

Reproductive Patterns and Social Organization of the Communal Guira Cuckoo (Guira guira) in Central Brazil

ABsTRACr.-The communal breeding system of the Guira Cuckoo (Guira guira) was studied near Brasilia, Brazil. Guiras occurred in groups of 2 to 13 adults (mode of 6) in the 86 nests observed. Communal clutch size was correlated with group size, an indirect indication that more birds contribute to the clutch in larger groups. Clutch size varied from 4 to 20 eggs, but usually fewer eggs were incubated than were laid, since egg tossing by the adults was common. The temporal patterns of egg laying and egg loss, while generally similar to those of other crotophagines, differed in some ways. Egg losses occur at any time after laying starts. Losses may occur after several eggs have accumulated in the nest, may affect only part of the clutch, and may happen close to, or during, the hatching of chicks. Only 26% of eggs developed into fledglings; high mortality rates for eggs and chicks are due to several causes. An individual may pay a price for group membership through a lowered short-term reproductive success; however, long-term data are needed to clarify individual lifetime benefits associated with communal breeding in this species. Received 18 June 1991, accepted 20 February 1992.

BREEDING STRATEGIES OF A SOCIALLY MONOGAMOUS NEOTROPICAL PASSERINE: EXTRA-PAIR FERTILIZATIONS, BEHAVIOR, AND MORPHOLOGY

Abstract Blue-black Grassquits (Volatinia jacarina) are small, granivorous, Neotropical birds that are abundant in central Brazil. During the reproductive season, the socially monogamous males acquire a blue-black plumage and defend very small, clustered territories that resemble leks. They execute a conspicuous courtship display that consists of a leap, revealing white under-wing patches, synchronized with a vocalization. We collected data on the morphology and behavior of banded males and characteristics of their territories to determine how these factors may influence acquisition of mates and nesting. For a second group of birds in the area, we used microsatellite genotyping to test the breeding synchrony hypothesis, which predicts that tropical species that breed synchronously should exhibit high rates of extra-pair fertilization (EPF). We found that males that successfully formed a pair bond differed from unsuccessful males in their behavior, but not in morphological attributes or territory features. Successful males spent more time in their territories, executed displays for longer periods and at greater rates, and their display leaps were higher. These results point to the greater importance of behavior relative to other factors in the successful reproduction of Blue-black Grassquit males. In the second group of birds, EPFs occurred in 63% of 11 nests and involved 50% of the 20 chicks sampled. This exceptionally high incidence of EPF in the small sample analyzed occurred in diverse contexts, including intraspecific parasitism and quasi-parasitism, a rare type of maternity loss where the resident female is parasitized by other females that were fertilized by the resident male. A short and highly synchronized breeding season, clustered breeding in small territories, and granivorous habits may contribute to the high rates of EPF in this tropical species.

LEK-LIKE MATING SYSTEM OF THE MONOGAMOUS BLUE-BLACK GRASSQUIT

Abstract In this study, we investigated the role of display and mating system of the little known Neotropical Blue-black Grassquit (Volatinia jacarina). Males form aggregations and execute a highly conspicuous display, resembling traditional leks. Number of displaying males declined throughout the study period, though displaying intensity during the season showed no variation. Individual males had significantly different displaying rates and also defended territories of very different sizes, ranging from 13.0 to 72.5 m2, but we found no association between territory sizes and the average displaying rates of the resident males. There also is no association between displaying rates of males and size and vegetation structure of their territories. Four of seven nests were found within male territories and observations indicated that both sexes invest equally in caring for nestlings. Results suggest that the Blue-black Grassquit does not fit into the traditional lek mating system, contrary to what has been proposed in the scarce literature available. However, it is clear that these apparently monogamous birds behave like a lekking species. We speculate about the possibility that aggregation of nesting territories in this species may be due to sexual selection pressures, and suggest that the Blue-black Grassquit may be an ideal candidate to test Wagners (1997) hidden-lek hypothesis.

Nanostructural self-assembly of iridescent feather barbules through depletion attraction of melanosomes during keratinization

Avian plumage colours are model traits in understanding the evolution of sexually selected ornamental traits. Paradoxically, iridescent structural colours, probably the most dazzling of these traits, remain the most poorly understood. Though some data suggest that expression of bright iridescent plumage colours produced by highly ordered arrays of melanosomes and keratin is condition-dependent, almost nothing is known of their ontogeny and thus of any developmental mechanisms that may be susceptible to perturbation. Here, we use light and electron microscopy to compare the ontogeny of iridescent male and non-iridescent female feathers in blue-black grassquits. Feather barbules of males contain a single layer of melanosomes bounded by a thin layer of keratin-producing blue iridescent colour, while those of females contain disorganized melanosomes and no outer layer. We found that nanostructural organization of male barbules occurs late in development, following death of the barbule cell, and is thus unlikely to be under direct cellular control, contrary to previous suggestions. Rather, organization appears to be caused by entropically driven self-assembly through depletion attraction forces that pin melanosomes to the edge of barbule cells and to one another. These forces are probably stronger in developing barbules of males than of females because their melanosomes are (i) larger, (ii) more densely packed, and (iii) more homogeneously distributed owing to the more consistent shape of barbules during keratinization. These data provide the first proposed developmental pathway for iridescent plumage colours, and suggest that any condition dependence of iridescent barbules is likely driven by factors other than direct metabolic cost.

Maternal androgens in eggs of communally breeding guira cuckoos (Guira guira)

Variation of maternal androgens in avian eggs may be a mechanism of maternal influence on offspring development, growth, and/or behavior. We studied yolk androgen concentrations in eggs of guira cuckoos (Guira guira) to understand how females might enhance the success of offspring in a complex communal breeding system. We measured concentrations of androstenedione, 5alpha-dihydrotestosterone, and testosterone in yolks and identified eggs and clutches of individuals in joint nests by yolk protein electrophoresis. Androstenedione had the highest yolk concentration, at least 10 times higher than that of testosterone and 5alpha-dihydrotestosterone. The first eggs of individual females that laid two or three eggs in a joint nest had lower androstenedione concentrations than their second and third eggs, the latter having a lower probability of being ejected from the nest. This implies that guira cuckoo females may influence offspring survival and competitiveness in communal nests by means of differential allocation of androstenedione and laying tactics. There was significant variation in yolk androstenedione among females, but the order in which females entered laying in the communal clutch had no effect on the concentrations. Androstenedione yolk concentrations increased with communal clutch size, which may indicate that higher levels of competition in larger groups lead to higher yolk androgen concentrations. Finally, androstenedione concentrations were higher in clutches in the later wetter periods of the rainy season than during the earlier drier period. This may be explained by the high frequency of large clutches in the later periods, with more females contributing to a joint clutch.

Breeding patterns and habitat use in the endemic Curl-crested Jay of central Brazil

Abstract Little is known about the life history and reproduction of the Curl-crested Jay (Cyanocorax cristatellus), despite its conspicuousness and endemic status, being restricted primarily to the central Cerrado biome of Brazil. From May 1999 to December 2000, we examined the sizes of home ranges and foraging and reproductive patterns in this species. Average group size was approximately 10 individuals, with average home ranges of 172 ha; during the reproductive period individuals in the group tended to stay within approximately 29 ha of active nests. These jays are dietary generalists, while the diversity of substrates and capture techniques employed showed high flexibility in resource utilization. The reproductive period was from September to March, and groups produced average clutch sizes of 5.7 eggs, but only 35% of these hatched and only 25% of the nests produced at least one fledgling. Predation was the chief cause of nesting failure, accounting for 63% of nest loss. The occurrence of large groups year-round with several individuals providing parental care and evidence of just one female laying eggs suggest that the Curl-crested Jay is a cooperative breeder with a high degree of sociality. However, further study is necessary to exclude the possibility that more than one female is laying eggs in a single nest.

CONTEXT AND FREQUENCY OF INFANTICIDE IN COMMUNALLY BREEDING GUIRA CUCKOOS

Abstract We studied the context of brood reduction through infanticide by communally breeding Guira Cuckoos (Guira guira) in central Brazil. During seven reproductive seasons, we monitored 142 nests from egg laying until fledging. Almost all nests (97%) lost eggs through ejection, and chick deaths occurred in 72% of all nests with hatchlings. There was evidence for infanticide in 38% of the nests that exhibited some mortality. We compared egg and chick mortality in the early part of the season with the later part, when insect abundance declines, but found no significant differences. Less than one-third of all nests monitored showed asynchronous hatching of eggs, and in those that did, chick death was not in reverse hatch order. Although there are several plausible explanations for infanticide, we highlight one likely candidate, which is its interpretation as a sexually selected trait where individuals gain reproductive benefits by provoking the groups nesting failure.