Jordan Karubian

COSTS AND BENEFITS OF VARIABLE BREEDING PLUMAGE IN THE RED-BACKED FAIRY-WREN

Abstract The red‐backed fairy‐wren is a socially monogamous passerine bird which exhibits two distinct types of breeding male, bright males that breed in bright red and black plumage and dull males that breed in dull brown plumage. Most males spe006Ed their first potential breeding season in dull plumage and subsequent breeding seasons in bright plumage, but a relatively small proportion of males develop bright plumage in their first breeding season. This study quantifies morphology, behavior, and reproductive success of dull and bright males to assess the adaptive costs and benefits of bright plumage while controlling for age. Older bright males (two years of age or older) attempted to increase their reproductive success via copulations with extra pair females, whereas younger (one‐year old) bright males and dull males did not. Thus, older bright males spent less time on their own territories, intruded on neighboring groups with fertile females more frequently, gave more courtship displays, and had larger sperm storage organs than did younger bright males and dull males. Micro satellite analyses of paternity indicate that the red‐backed fairy‐wren has extremely high levels of sexual promiscuity, and that older bright males had higher within‐brood paternity than dull males or younger bright males. Regardless of age, bright males were more attractive to females in controlled mate choice trials than were dull males, and both age classes of bright males obtained higher quality mates earlier in the breeding season than did dull males, when nesting success was higher. In conclusion, although it appears that bright plumage increases access to higher quality mates, age also plays a central role in determining a males overall reproductive success because of the high levels of sexual promiscuity exhibited by the red‐backed fairy‐wren.

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

Destination-based seed dispersal homogenizes genetic structure of a tropical palm.

As the dominant seed dispersal agents in many ecosystems, frugivorous animals profoundly impact gene movement and fine‐scale genetic structure of plants. Most frugivores engage in some form of destination‐based dispersal, in that they move seeds towards specific destinations, resulting in clumped distributions of seeds away from the source tree. Molecular analyses of dispersed seeds and seedlings suggest that destination‐based dispersal may often yield clusters of maternal genotypes and lead to pronounced local genetic structure. The long‐wattled umbrellabird Cephalopterus penduliger is a frugivorous bird whose lek mating system creates a species‐specific pattern of seed dispersal that can potentially be distinguished from background dispersal processes. We used this system to test how destination‐based dispersal by umbrellabirds into the lek affects gene movement and genetic structure of one of their preferred food sources Oenocarpus bataua, a canopy palm tree. Relative to background dispersal processes, umbrellabird mating behaviour yielded more diverse seed pools in leks that included on average five times more seed sources and a higher incidence of long‐distance dispersal events. This resulted in markedly lower fine‐scale spatial genetic structure among established seedlings in leks than background areas. These species‐specific impacts of destination‐based dispersal illustrate how detailed knowledge of disperser behaviour can elucidate the mechanistic link driving observed patterns of seed movement and genetic structure.

GENOMIC AND MORPHOLOGICAL ANALYSIS OF A SEMIPERMEABLE AVIAN HYBRID ZONE SUGGESTS ASYMMETRICAL INTROGRESSION OF A SEXUAL SIGNAL

Hybrid zones are geographic regions where differentiated taxa meet and potentially exchange genes. Increasingly, genomic analyses have demonstrated that many hybrid zones are semipermeable boundaries across which introgression is highly variable. In some cases, certain alleles penetrate across the hybrid zone in only one direction, recombining into the alternate genome. We investigated this phenomenon using genomic (genotyping‐by‐sequencing) and morphological (plumage reflectance spectrophotometry) analyses of the hybrid zone between two subspecies of the red‐backed fairy‐wren (Malurus melanocephalus) that differ conspicuously in a sexual signal, male back plumage color. Geographic cline analyses revealed a highly variable pattern of differential introgression, with many narrow coincident clines combined with several significantly wider clines, suggesting that the hybrid zone is a semipermeable tension zone. The plumage cline was shifted significantly into the genomic background of the orange subspecies, consistent with sexual selection driving asymmetrical introgression of red plumage alleles across the hybrid zone. This interpretation is supported by previous experimental work demonstrating an extra‐pair mating advantage for red males, but the role of genetic dominance in driving this pattern remains unclear. This study highlights the potential for sexual selection to erode taxonomic boundaries and promote gene flow, particularly at an intermediate stage of divergence.

Bill coloration, a flexible signal in a tropical passerine bird, is regulated by social environment and androgens

Although some group-living animals dynamically modify sexual signals in response to changes in social or reproductive status, this ability is often limited by constraints inherent in the mechanism of signal production. In birds, for example, inflexible moult schedules may restrict the ability to rapidly modify plumage-based signals. In such cases, more flexible secondary signals such as skin, eye, or bill coloration (e.g. soft parts) could potentially be used to achieve dynamic signalling. We addressed the degree to which free-living red-backed fairy-wrens, Malurus melanocephalus, can dynamically update both plumage and soft part signals when status suddenly changes, and how this may be achieved. In this cooperatively breeding passerine, dominant breeding males are distinguished from socially subordinate nonbreeding auxiliary males by the presence of nuptial plumage, dark bills and large sperm storage organs. Following an experimentally induced shift in status from auxiliary to breeder, males showed rapid increases in excreted androgen metabolites. Although they showed no overall change in nuptial plumage colour, several experimental males developed red nuptial feathers on the back following feather plucking, indicating that they had the capacity to develop bright nuptial plumage but were constrained from doing so by the moult schedule. In contrast, experimental males showed a rapid darkening of their bills, reflecting their newly acquired breeding status. These findings (1) provide experimental evidence that status affects physiologically controlled visual signals in free-living birds, (2) suggest that this linkage is mediated by testosterone and (3) illustrate how secondary ornaments may be used in dynamic signalling when the primary signalling modality is constrained.

The pollen dispersal kernel and mating system of an insect-pollinated tropical palm, Oenocarpus bataua

Pollen dispersal shapes the local genetic structure of plant populations and determines the opportunity for local selection and genetic drift, but has been well studied in few animal-pollinated plants in tropical rainforests. Here, we characterise pollen movement for an insect-pollinated Neotropical canopy palm, Oenocarpus bataua, and relate these data to adult mating system and population genetic structure. The study covers a 130-ha parcel in which all adult trees (n=185) were mapped and genotyped at 12 microsatellite loci, allowing us to positively identify the source tree for 90% of pollination events (n=287 of 318 events). Mating system analysis showed O. bataua was effectively outcrossed (tm=1.02) with little biparental inbreeding (tm−ts=−0.005) and an average of 5.4 effective pollen donors (Nep) per female. Dispersal distances were relatively large for an insect-pollinated species (mean=303 m, max=1263 m), and far exceeded nearest-neighbour distances. Dispersal kernel modelling indicated a thin-tailed Weibull distribution offered the best fit to the genetic data, which contrasts with the fat-tailed kernels typically reported for pollen dispersal in trees. Preliminary analyses suggest that our findings may be explained, at least in part, by a relatively diffuse spatial and temporal distribution of flowering trees. Comparison with previously reported estimates of seed movement for O. bataua suggests that pollen and seed dispersal distances may be similar. These findings add to the growing body of information on dispersal in insect-pollinated trees, but underscore the need for continued research on tropical systems in general, and palms in particular.

TEMPORAL AND SPATIAL PATTERNS OF MACAW ABUNDANCE IN THE ECUADORIAN AMAZON

Abstract Although macaws are arguably the most widely recognized species of bird from Neotropical rainforests, little is known of their basic biology or demography in the wild. In Ecuador, as in other Neotropical countries, it is suspected that several species of macaw are declining in response to human activity and habitat alteration but there is little hard data supporting this supposition. In this paper, we present one full year of data on macaw populations from a relatively pristine site in the Ecuadorian Amazon, and compare this site to two other sites with intermediate and relatively high levels of human activity. At Tiputini Biodiversity Station, a pristine terra-firme forest, macaws were more common in the dry season than in the wet season. This pattern is the opposite of that recently reported for seasonally inundated forests in Peru, suggesting that macaws may make large-scale, seasonal movements across habitat types. We employed the same sampling methodology for shorter periods of time at Sacha Lodge, characterized by intermediate levels of human activity, and at Jatun Sacha Biological Station, characterized by relatively high levels of human activity and habitat degradation. We recorded an intermediate number of macaws at Sacha Lodge, and the lowest densities at Jatun Sacha. Three groups of indicator taxa sampled at all three sites showed a similar pattern. These data provide a baseline for future demographic studies of macaws in the Ecuadorian Amazon and lend tentative support to the idea that macaw population declines may be linked to human activity and habitat alteration. Patrones Temporales y Espaciales de Abundancia de Guacamayos en la Amazonía Ecuatoriana Resumen. A pesar de que los guacamayos son en principio el grupo de especies de aves más conspicuo de los bosques neotropicales, muy poco se sabe sobre su biología básica y demografía en estado silvestre. En Ecuador, como en otros países neotropicales, se sospecha que algunas especies de guacamayos están desapareciendo en respuesta a la actividad humana y a la alteración del hábitat, aunque hay muy poca información que sustente esta suposición. En este trabajo, presentamos información sobre la demografía de los guacamayos obtenida durante un período de un año en un lugar relativamente prístino de la amazonía ecuatoriana, y lo comparamos con dos lugares que poseen niveles intermedios y altos de alteración humana. En la Estación de Biodiversidad Tiputini, un lugar con bosques de tierra firme en estado relativamente prístino, los guacamayos fueron más comunes en la temporada seca que en la temporada lluviosa. Este patrón es opuesto a lo reportado en bosques estacionalmente inundados en Perú, sugiriendo que los guacamayos podrían realizar desplazamientos estacionales a gran escala a través de diferentes tipos de hábitat. Nosotros empleamos la misma metodología de muestreo durante períodos más cortos de tiempo en Sacha Lodge, un lugar caracterizado por un nivel intermedio de impacto humano, y en la Estación Biológica Jatun Sacha, caracterizada por niveles de impacto humano y alteración de hábitat relativamente altos. Registramos un número intermedio de guacamayos en Sacha Lodge y densidades bajas en la Estación Biológica Jatun Sacha. Otros tres grupos de indicadores taxonómicos muestreados en los tres lugares visitados mostraron un patrón similar. Esta información provee una línea de base para futuros estudios demográficos de los guacamayos en la amazonía ecuatoriana y respalda de modo tentativo la idea de que la disminución de las poblaciones de guacamayos podría estar relacionada con la actividad humana y la alteración del hábitat.

A Trans-Amazonian Screening of mtDNA Reveals Deep Intraspecific Divergence in Forest Birds and Suggests a Vast Underestimation of Species Diversity

The Amazonian avifauna remains severely understudied relative to that of the temperate zone, and its species richness is thought to be underestimated by current taxonomy. Recent molecular systematic studies using mtDNA sequence reveal that traditionally accepted species-level taxa often conceal genetically divergent subspecific lineages found to represent new species upon close taxonomic scrutiny, suggesting that intraspecific mtDNA variation could be useful in species discovery. Surveys of mtDNA variation in Holarctic species have revealed patterns of variation that are largely congruent with species boundaries. However, little information exists on intraspecific divergence in most Amazonian species. Here we screen intraspecific mtDNA genetic variation in 41 Amazonian forest understory species belonging to 36 genera and 17 families in 6 orders, using 758 individual samples from Ecuador and French Guiana. For 13 of these species, we also analyzed trans-Andean populations from the Ecuadorian Chocó. A consistent pattern of deep intraspecific divergence among trans-Amazonian haplogroups was found for 33 of the 41 taxa, and genetic differentiation and genetic diversity among them was highly variable, suggesting a complex range of evolutionary histories. Mean sequence divergence within families was the same as that found in North American birds (13%), yet mean intraspecific divergence in Neotropical species was an order of magnitude larger (2.13% vs. 0.23%), with mean distance between intraspecific lineages reaching 3.56%. We found no clear relationship between genetic distances and differentiation in plumage color. Our results identify numerous genetically and phenotypically divergent lineages which may result in new species-level designations upon closer taxonomic scrutiny and thorough sampling, although lineages in the tropical region could be older than those in the temperate zone without necessarily representing separate species. In-depth phylogeographic surveys are urgently needed to avoid underestimating tropical diversity, and the use of mtDNA markers can be instrumental in identifying and prioritizing taxa for species discovery.

Offspring sex ratios reflect lack of repayment by auxiliary males in a cooperatively breeding passerine

The repayment hypothesis posits that primary sex ratios in cooperative species should be biased towards the helping sex because these offspring “repay” a portion of their cost through helping behavior and therefore are less expensive to produce. However, many cooperatively breeding birds and mammals do not show the predicted bias in the primary sex ratio. Recent theoretical work has suggested that the repayment hypothesis should only hold when females gain a large fitness advantage from the presence of auxiliary adults in the group. When auxiliaries provide little or no fitness advantage, competition between relatives should lead to sex ratios biased towards the dispersing (non-helping) sex. We examined the benefits auxiliaries provide to females and corresponding offspring sex ratios in the red-backed fairy-wren (Malurus melanocephalus), a cooperatively breeding Australian bird with male auxiliary helpers. We found that auxiliaries provide little or no benefit to female reproductive success or survival. As predicted, the population primary sex ratio was biased towards daughters, the dispersing sex, and females with auxiliaries produced female-biased broods whereas females without auxiliaries produced unbiased broods. Moreover, offspring sex ratios were more strongly biased toward females in years when auxiliaries were more common in the population. These results suggest that offspring sex ratios are associated with competition among the non-dispersing sex in this species, and also that females may use cues to assess local breeding opportunities for their offspring.

Use of Alpha, Beta, and Gamma Diversity Measures to Characterize Seed Dispersal by Animals

Seed dispersal shapes ecological and evolutionary dynamics of plant populations. Here, we extend classical diversity measures to study the impact of disperser behavior on seed dispersal. We begin by extending our previous diversity structure approach, which partitioned seed source diversity within and among dispersal sites, into the more general framework of traditional diversity measures. This statistical approach allows an assessment of the extent to which foraging behavior shapes α and γ diversity, as well as the divergence in seed sources among dispersal sites, which we call δ. We also introduce tests to facilitate comparisons of diversity among dispersal sites and seed vectors and to compare overall diversity among sampled systems. We then apply these tools to investigate the diversity blend of parentage resulting from seed dispersal by two avian seed vectors with very different social and foraging behaviors: (1) acorn woodpeckers, transporting Quercus agrifolia acorns, and (2) long-wattled umbrellabirds, transporting Oenocarpus bataua palm nuts. Using these diversity and divergence measures, we test the hypothesis that different foraging behaviors generate distinctive diversity partitions for the two focal tree species. This approach provides a new tool for assessment of the impact of dispersal agents on the seed source structure of plant populations, which can be extended to include the impact of virtually any propagule vector for a range of systems.