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

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.

[1]  J. Chaves-Campos,et al.  The effect of local dominance and reciprocal tolerance on feeding aggregations of ocellated antbirds , 2009, Proceedings of the Royal Society B: Biological Sciences.

[2]  S. Nowicki,et al.  Swamp sparrows modulate vocal performance in an aggressive context , 2009, Biology Letters.

[3]  H. Kokko,et al.  Evolution of Mate Choice for Genome-Wide Heterozygosity , 2009, Evolution; international journal of organic evolution.

[4]  J. Chaves-Campos,et al.  The spatial distribution of avian relatives: do obligate army‐ant‐following birds roost and feed near family members? , 2008, Molecular ecology.

[5]  Franz Goller,et al.  Frequency modulation during song in a suboscine does not require vocal muscles. , 2008, Journal of neurophysiology.

[6]  O. Gimenez,et al.  Genetic Heterozygosity and Sociality in a Primate Species , 2008, Behavior genetics.

[7]  T. Janicke,et al.  Vocal performance reflects individual quality in a nonpasserine , 2008, Animal Behaviour.

[8]  J. Atwell,et al.  Inferring performance in the songs of dark-eyed juncos (Junco hyemalis) , 2007 .

[9]  E. A. MacDougall-Shackleton,et al.  Song repertoire size varies with HVC volume and is indicative of male quality in song sparrows (Melospiza melodia) , 2007, Proceedings of the Royal Society B: Biological Sciences.

[10]  J. Aparicio,et al.  Egg production and individual genetic diversity in lesser kestrels , 2007, Molecular ecology.

[11]  D. Reby,et al.  Communication of Male Quality in Owl Hoots* , 2007, The American Naturalist.

[12]  J. Weber,et al.  Effects of genome-wide heterozygosity on a range of biomedically relevant human quantitative traits. , 2007, Human molecular genetics.

[13]  J. Aparicio,et al.  What should we weigh to estimate heterozygosity, alleles or loci? , 2006, Molecular ecology.

[14]  M. Hall,et al.  Vocal performance influences male receiver response in the banded wren , 2006, Proceedings of the Royal Society B: Biological Sciences.

[15]  M. Webster,et al.  Montezuma oropendolas modify a component of song constrained by body size during vocal contests , 2006, Animal Behaviour.

[16]  S. Nowicki,et al.  The Evolution of Animal Communication: Reliability and Deception in Signaling Systems: Reliability and Deception in Signaling Systems , 2005 .

[17]  T. Clutton‐Brock,et al.  Red deer stags use formants as assessment cues during intrasexual agonistic interactions , 2005, Proceedings of the Royal Society B: Biological Sciences.

[18]  J. DeWoody,et al.  On the estimation of genome-wide heterozygosity using molecular markers. , 2005, The Journal of heredity.

[19]  N. Seddon ECOLOGICAL ADAPTATION AND SPECIES RECOGNITION DRIVES VOCAL EVOLUTION IN NEOTROPICAL SUBOSCINE BIRDS , 2005, Evolution; international journal of organic evolution.

[20]  Benjamin N. Taft,et al.  Bird Song: The Interface of Evolution and Mechanism , 2004 .

[21]  D. Lesbarrères,et al.  Environmental and population dependency of genetic variability‐fitness correlations in Rana temporaria , 2004, Molecular ecology.

[22]  P. Marler,et al.  Nature's Music: The Science of Birdsong , 2004 .

[23]  R. Suthers Chapter 9 – How birds sing and why it matters , 2004 .

[24]  R. Mulder,et al.  Male heterozygosity predicts territory size, song structure and reproductive success in a cooperatively breeding bird , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[25]  C. Catchpole,et al.  Sexual selection and individual genetic diversity in a songbird , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  L. Keller,et al.  Inbreeding depresses immune response in song sparrows (Melospiza melodia): direct and inter–generational effects , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[27]  W. Amos,et al.  Inbreeding: Disease susceptibility in California sea lions , 2003, Nature.

[28]  M. Kreutzer,et al.  Directional female preference for an exaggerated male trait in canary (Serinusanaria) song , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[29]  B. Hansson,et al.  On the correlation between heterozygosity and fitness in natural populations , 2002, Molecular ecology.

[30]  O. Hardy,et al.  spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels , 2002 .

[31]  L. Keller,et al.  Inbreeding effects in wild populations. , 2002 .

[32]  Manfred Gahr,et al.  The honesty of bird song: multiple constraints for multiple traits , 2002 .

[33]  J. Croxall,et al.  The influence of parental relatedness on reproductive success , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[34]  F Goller,et al.  The neuromuscular control of birdsong. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[35]  P. Tubaro,et al.  Acoustic frequencies and body mass in new world doves , 1998 .

[36]  D. Kroodsma,et al.  Ecology and evolution of acoustic communication in birds , 1997 .

[37]  J. Podos A PERFORMANCE CONSTRAINT ON THE EVOLUTION OF TRILLED VOCALIZATIONS IN A SONGBIRD FAMILY (PASSERIFORMES: EMBERIZIDAE) , 1997, Evolution; international journal of organic evolution.

[38]  F Goller,et al.  Role of syringeal muscles in controlling the phonology of bird song. , 1996, Journal of neurophysiology.

[39]  A. Horn,et al.  Crowing in relation to status in roosters , 1995, Animal Behaviour.

[40]  William E. Wagner Deceptive or honest signalling of fighting ability? A test of alternative hypotheses for the function of changes in call dominant frequency by male cricket frogs , 1992, Animal Behaviour.

[41]  T R Tiersch,et al.  On the evolution of genome size of birds. , 1991, The Journal of heredity.

[42]  A. Møller Parasite load reduces song output in a passerine bird , 1991, Animal Behaviour.

[43]  D. Kroodsma Using appropriate experimental designs for intended hypotheses in ‘song’ playbacks, with examples for testing effects of song repertoire sizes , 1990, Animal Behaviour.

[44]  A. Grafen Biological signals as handicaps. , 1990, Journal of theoretical biology.

[45]  Eliot A. Brenowitz,et al.  The Role of Body Size, Phylogeny, and Ambient Noise in the Evolution of Bird Song , 1985, The American Naturalist.

[46]  W. Klitz,et al.  Allozymic heterozygosity and morphological variation in house sparrows , 1983, Nature.

[47]  D. Wallschläger,et al.  Correlation of song frequency and body weight in passerine birds , 1980, Experientia.

[48]  N. Davies,et al.  Deep croaks and fighting assessment in toads Bufo bufo , 1978, Nature.

[49]  A. Zahavi Mate selection-a selection for a handicap. , 1975, Journal of theoretical biology.

[50]  H. N. Barber Selection in natural populations , 1965, Heredity.

[51]  J. Podos,et al.  Vocal Performance and Sensorimotor Learning in Songbirds , 2009 .

[52]  J. Podos,et al.  Chapter 5 Vocal Performance and Sensorimotor Learning in Songbirds , 2009 .

[53]  J. L. Tomkins,et al.  On the resolution of the lek paradox. , 2008, Trends in ecology & evolution.

[54]  B. Byers Extrapair paternity in chestnut-sided warblers is correlated with consistent vocal performance , 2007 .

[55]  NEW TITLES , 2006 .

[56]  S. Nowicki,et al.  Vocal performance influences female response to male bird song: an experimental test , 2004 .

[57]  Jerram L. Brown A theory of mate choice based on heterozygosity , 1997 .

[58]  M. Andersson,et al.  SEXUAL SELECTION AND THE EVOLUTION OF SONG , 1986 .

[59]  D. Kroodsma Songs of the Alder Flycatcher (Empidonax alnorum) and Willow Flycatcher (Empidonax traillii) are Innate , 1984 .

[60]  E. Willis,et al.  The behavior of ocellated antbirds , 1973 .