High-Pitched Notes during Vocal Contests Signal Genetic Diversity in Ocellated Antbirds

University of Sussex, United Kingdom
PLoS ONE (Impact Factor: 3.53). 12/2009; 4(12):e8137. DOI: 10.1371/journal.pone.0008137
Source: PubMed

ABSTRACT Animals use honest signals to assess the quality of competitors during aggressive interactions. Current theory predicts that honest signals should be costly to produce and thus reveal some aspects of the phenotypic or genetic quality of the sender. In songbirds, research indicates that biomechanical constraints make the production of some acoustic features costly. Furthermore, recent studies have found that vocal features are related to genetic diversity. We linked these two lines of research by evaluating if constrained acoustic features reveal male genetic diversity during aggressive interactions in ocellated antbirds (Phaenostictus mcleannani). We recorded the aggressive vocalizations of radiotagged males at La Selva Biological Station in Costa Rica, and found significant variation in the highest frequency produced among individuals. Moreover, we detected a negative relationship between the frequency of the highest pitched note and vocalization duration, suggesting that high pitched notes might constrain the duration of vocalizations through biomechanical and/or energetic limitations. When we experimentally exposed wild radiotagged males to simulated acoustic challenges, the birds increased the pitch of their vocalization. We also found that individuals with higher genetic diversity (as measured by zygosity across 9 microsatellite loci) produced notes of higher pitch during aggressive interactions. Overall, our results suggest that the ability to produce high pitched notes is an honest indicator of male genetic diversity in male-male aggressive interactions.

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    • "Recent years have seen a wealth of papers describing heterozygosity–fitness correlations (HFCs) in which heterozygosity , usually measured at around 10 microsatellite markers, is shown to predict some aspect of an individual's fitness. The direction of the relationship seems almost invariably to be in the direction of higher heterozygosity indicating higher quality, and the traits studied embrace almost all aspects of life, from birth weight (Coulson et al. 1999) and parasite resistance (Rijks et al. 2008) though recruitment and reproductive and success (Amos et al. 2001; Cohas et al. 2009) to plumage coloration (Foerster et al. 2003), song pitch (Araya-Ajoy et al. 2009), attractiveness (Hoffman, Forada, et al. 2007), dominance status (Tiira et al. 2006) and territory holding ability (Höglund et al. 2002). As such, HFCs appear to represent an important component of fitness in many or perhaps even most systems. "
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    ABSTRACT: Although heterozygosity-fitness correlations (HFCs) are widely reported in the literature, most studies use too few markers to allow the proximate mechanisms to be convincingly resolved. Two competing hypotheses have been proposed: the general effect hypothesis, in which marker heterozygosity correlates with genome-wide heterozygosity and hence the inbreeding coefficient f, and the local effect hypothesis, in which one or more of the markers by chance exhibit associative overdominance. To explore the relative contributions of general and local effects in a free-ranging marine mammal population, we revisited a strong HFC found using 9 microsatellite loci for canine tooth size in 84 male Antarctic fur seals Arctocephalus gazella (Hoffman JI, Hanson N, Forcada J, Trathan PN, Amos W. 2010. Getting long in the tooth: a strong positive correlation between canine size and heterozygosity in the Antarctic fur seal Arctocephalus gazella. J Hered.). Increasing the number of markers to 76, we find that heterozygosity is uncorrelated across loci, indicating that inbred individuals are rare or absent. Similarly, while the HFC based on overall heterozygosity is lost, stochastic simulations indicate that when an HFC is due to inbreeding depression, increasing marker number invariably strengthens the HFC. Together these observations argue strongly that the original HFC was not due to inbreeding depression. In contrast, a subset of markers show individually significant effects, and these are nonrandomly distributed across the marker panel, being preferentially associated with markers cloned from other species. Using basic alignment search tool searches, we were able to locate 94% of loci to unique locations in the dog genome, but the local genes are functionally diverse, and the majority cannot be linked directly to growth. Our results suggest that inbreeding depression contributes little if at all to the relationship between heterozygosity and tooth size but that instead the primary mechanism involves associative overdominance. These findings contribute to a growing body of evidence suggesting that general effects are likely to be uncommon in natural populations.
    The Journal of heredity 05/2010; 101(5):539-52. DOI:10.1093/jhered/esq046 · 1.97 Impact Factor
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    ABSTRACT: In many animal species, the frequency (pitch) of vocalisations correlates negatively with body size and may thus signal competitive ability. However, this relationship is absent in other species. Understanding why this difference exists across species may help to explain some of the diversity of vocal communication systems. We assessed whether vocalisation frequency signals body size in black swans (Cygnus atratus), and how this is affected by (i) variation in frequency within individuals and (ii) size variation across individuals. Frequency was correlated with body size and mass, with slopes close to the allometry expected if the birds were maximising sound radiation, but the explained variation in frequency was low. Within-individual variation in vocalisation frequency was greater in male than female swans, and the reliability of frequency as a signal of size in males was correspondingly lower. A review of the literature on the relationship between the frequency of avian vocalisations and body size also showed smaller effect sizes for more variable vocalisations (birdsongs), than for simpler vocalisations. Vocalisation frequency was more reliably correlated with body size when the sexes were pooled (creating a larger range of variation in size) than when the relationship was examined for either sex separately, although male and female data followed the same allometric line. These results show that variation in frequency within individuals and low variation in size across individuals reduce the reliability of vocalisation frequency as a signal of body size, which helps to understand differences among species in the signal value of vocalisation frequency.
    Ethology 03/2010; 116(6):554 - 563. DOI:10.1111/j.1439-0310.2010.01769.x · 1.56 Impact Factor
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    ABSTRACT: Most studies of heterozygosity-fitness correlations (HFCs) in natural populations relate to fitness traits expressed early in life, whereas traits that are often more difficult to measure such as longevity and adult body size remain elusive. Teeth provide a window on an individual's life history, allowing the reliable estimation of both age and body size. Consequently, we collected paired upper canine teeth and tissue samples from 84 adult male Antarctic fur seals Arctocephalus gazella that died of natural causes at Bird Island, South Georgia. Tooth size is a good predictor of skull and body size both within and across taxa, and we similarly find a strong relationship with skull size in our species. In turn, tooth size is itself predicted strongly by genetic heterozygosity estimated using 9 microsatellites. With only 9 loci, the exact mechanisms involved remain unclear, although the observed pattern appears largely attributable to a small subset of loci, suggesting that associative overdominance rather than inbreeding depression provides the proximate mechanism. In addition, locating these markers in the dog genome reveals proximity to genes involved with fat metabolism and growth. Our study illustrates how canine teeth, and potentially other structures such as tympano-periotic bone, waxy inner earplugs, or otoliths, may be used to explore links between genetic variation and important life-history traits in free-ranging vertebrate populations.
    The Journal of heredity 05/2010; 101(5):527-38. DOI:10.1093/jhered/esq045 · 1.97 Impact Factor
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