Reconstrucción de las características de historia de vida en los ancestros de los tordos: un análisis de las adaptaciones al parasitismo de cría

E. Manuela Pujol; Myriam E. Mermoz

doi:10.56178/eh.v21i1.794

Articles Published 01 August 2006 https://doi.org/10.56178/eh.v21i1.794

Reconstruction of ancestral states of life-history traits in cowbirds: an analysis of adaptations to brood parasitism

adaptation ancestor reconstruction cowbirds eggshell thickness egg weight incubation period nestling growth

E. Manuela Pujol Laboratorio de Ecología y Comportamiento Animal, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires. Piso 4, Pab. 2, Ciudad Universitaria, C1428EHA Buenos Aires, Argentina

Myriam E. Mermoz Laboratorio de Ecología y Comportamiento Animal, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires. Piso 4, Pab. 2, Ciudad Universitaria, C1428EHA Buenos Aires, Argentina

Abstract

Parasitic cowbirds lay their eggs in the nest of other species, the host, depending on the host’s parental care for their successful reproduction. It has been suggested that cowbirds modified some life-history traits as adaptations to brood parasitism. Specifically, they would have developed small-sized eggs with thicker eggshells, would have shortened their incubation periods, and would have accelerated nestling growth. A previous analysis with independent phylogenetic contrasts found that observed values of those life-history traits in parasitic cowbirds only differ from the predicted ones by their non-parasitic relatives in their thicker eggshell. In this work, we reanalyzed these traits as potential adaptations to brood parasitism in cowbirds by reconstructing ancestral values under two models of character evolution. By comparing the ancestors reconstructed from the parasitic cowbirds with those reconstructed from their non-parasitic relatives, we only found differences in eggshell thickness. This demonstrates that both techniques (ancestor reconstruction and independent phylogenetic contrasts) are consistent, and that the increase in eggshell thickness as a potential adaptation to brood parasitism is a robust result.

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References

ARAGÓN S, MOLLER AP, SOLER JJ Y SOLER M (1999)Molecular phylogeny of cuckoos supports a poly-phyletic origin of brood parasitism. Journal of Evolu-tionary Biology 12:495–506
BJÖRKLUND M (1997) Are “comparative methods” al-ways necessary? Oikos 80:607–612
BROOKER LC Y BROOKER MG (1991) Eggshell strengthin cuckoos and cowbirds. Ibis 133:406–413
CADENA CD, CUERVO AM Y LANYON SM (2004) Phy-logenetic relationships of the red-bellied grackle(Icteridae: Hyppyrrhus pyrohypogaster) inferredfrom mitochondrial DNA sequence data. Condor106:664–671
CARTER MD (1986) The parasitic behavior of thebronzed cowbird in south Texas. Condor 88:11–25
CLAYTON NS, REBOREDA JC Y KACELNIK A (1997) Sea-sonal change of hippocampus volume in parasiticcowbirds. Behavioral Processes 41:237–243
DAVIES NB (2000) Cuckoo, cowbirds and other cheats.Academic Press, Londres
DAVIES NB Y BROOKE LC (1989) An experimental studyof co-evolution between the cuckoo, Cuculus canarusand its host. II. Host egg markings, chick discrimi-nation and general discussion. Journal of AnimalEcology 58:225–236
FELSENSTEIN J (1985) Phylogenies and the compara-tive data. American Naturalist 125:1–15
FRAGA RM (1998) Interactions of the parasitic scream-ing and shiny cowbirds (Molothrus rufoaxillaris andM. bonariensis) with a shared host, the bay-wingedcowbird (Molothrus badius). Pp. 173–193 en:ROTHSTEIN SI Y ROBINSON SK (eds) Parasitic birds andtheir hosts: studies in coevolution. Oxford UniversityPress, Nueva York
FRAGA RM Y DI GIACOMO A (2004) Cooperative breed-ing of the yellow-rumped marshbird (Icteridae) inArgentina and Paraguay. Condor 106:671–673
FRIEDMANN H (1929) The cowbirds, a study in the biologyof the social parasitism. CC Thomas, Springfield
FRIEDMANN H (1960) The parasitic weaverbirds. UnitedStates National Museum Bulletin 223:1–196
GARLAND JR T Y ADOLPH SC (1994) Why not to do twospecies comparative studies: limitations on inferringadaptations. Physiological Zoology 67:797–828
GARLAND JR T, BENNETT A Y REZENDE EL (2005) Phylo-genetic approaches in comparative physiology.Journal of Experimental Biology 208:3015–3035
GARLAND JR T E IVES AR (2000) Using the past to pre-dict the present: confidence intervals for regressionequation in phylogenetic comparative methods.American Naturalist 155:346–364
GARLAND JR T, MARTIN KML Y DÍAZ-URIARTE R (1997)Reconstructing ancestral trait values using squared-change parsimony: plasma osmolarity at the originof amniotes. Pp. 425–501 en: SUMIDA SS y MARTINKLM (eds) Amniote origins: completing the transitionto land. Academic Press, San Diego
GARLAND JR T, MIDFORD PE E IVES AR (1999) An intro-duction to phylogenetically based statistical meth-ods, with a new method for confidence intervalson ancestral states. American Zoology 39:374–388
GOULD SJ Y VBRA ES (1982) Exaptation —a missingterm in the science of form. Paleobiology 8:4–15
GRIM T (2005) Mimicry vs. similarity: which resem-blances between brood parasites and their hosts aremimetic and which are not? Biological Journal of theLinnean Society 84:69–78
HUDSON WH (1874) Notes on the procreant instinctsof the three species of Molothrus found in BuenosAyres. Proceedings of the Zoological Society of London9:153–174
JOHNSON KP Y LANYON SM (1999) Molecular system-atics of the grackles and allies, and effect of addi-tional sequence (Cyt b and ND2). Auk 116:759–768
KATTAN GH (1995) Mechanism of short incubationperiod in brood parasitic cowbirds. Auk 112:335–342
KATTAN GH (1996) Growth and provisioning of shinycowbirds and house wren host nestling. Journal ofField Ornithology 67:434–441
LANYON SM (1992) Interspecific brood parasitism inblackbirds (Icterinae): a phylogenetic perspective.Science 225:77–79
MADDISON WP (1991) Squared-changed parsimonyreconstruction of ancestral states for continuous-valued character on a phylogenetic tree. SystematicZoology 40:304–314
MARTINS EP (1999) Estimation of ancestral states ofcontinuous character: a computer simulation study.Systematic Biology 48:642–650
MARTINS EP Y GARLAND JR T (1991) Phylogenetic analy-ses of the correlated evolution of continuous char-acter: a simulation study. Evolution 45:534–557
MASON P (1986) Brood parasitism in a host general-ist, the Shiny Cowbird: I. The quality of differentspecies as hosts. Auk 103:52–60
MERMOZ ME (1996) Interacciones entre el tordo renegri-do Molothrus bonariensis y el pecho amarillo Pseudoleistesvirescens: estrategias del parásito de cría y mecanismosde defensa del hospedador. Tesis doctoral, Universidadde Buenos Aires, Buenos Aires
MERMOZ ME Y ORNELAS JF (2004) Phylogenetic analy-sis of life-history adaptations in parasitic cowbirds.Behavioral Ecology 15:109–119
MERMOZ ME Y REBOREDA JC (1999) Egg layingbehaviour by shiny cowbirds parasitizing brown-and-yellow marshbirds. Animal Behaviour 58:873–882
OAKLEY TH Y CUNNINGHAM CW (2000) Independent con-trasts succeed where ancestor reconstruction fails inknown bacteriophage phylogeny. Evolution 54:397–405
ORTEGA CP Y CRUZ A (1992) Differential growth pat-terns of nestling brown-headed cowbirds and yel-low-headed blackbirds. Auk 109:368–376
PAYNE RB (1973) Individual laying histories and theclutch size and numbers of eggs of parasitic cuck-oos. Condor 75:414–438
PAYNE RB (1977) The ecology of brood parasitism inbirds. Annual Review of Ecology and Systematics 8:1–28
PAYNE RB, PAYNE LL Y WOODS JL (2000) Imprintingand the origin of parasite-host species associationsin brood-parasitic indigobirds, Vidua chalybeata.Animal Behaviour 59:69–81
PUJOL EM (2005) Evolución de las características dehistoria de vida en el grupo que dio origen a los tordosparásitos (Aves: Icteridae). Tesis de Licenciatura, Uni-versidad de Buenos Aires, Buenos Aires
RAHN H, CURRAN-EVERET L Y BOOTH DT (1988) Egg-shell differences between parasitic and nonparasiticIcteridae. Condor 90:962–964REEVE HK Y SHERMAN PW (1993) Adaptation and thegoals of evolutionary research. Quarterly Review ofBiology 68:1–31
REZENDE EL Y GARLANDJR T (2003) Comparacionesinterespecíficas y métodos estadísticos filogenéticos.Pp. 79–98 en: BOZINOVIC F (ed) Fisiología ecológica yevolutiva. Teoría y casos de estudio en animales. Edicio-nes Universidad Católica de Chile, Santiago
ROHWER S Y SPA W CD (1988) Evolutionary lag versusbill-size constraints: a comparative study of theacceptance of cowbirds eggs by old hosts. Evolution-ary Ecology 2:27–36
ROTHSTEIN SI (1990) A model system for coevolution:avian brood parasitism. Annual Review of Ecology andSystematics 21:481–508
ROTHSTEIN SI Y ROBINSON SK (1998) The evolution andecology of avian brood parasitism: an overview. Pp.3–58 en: ROTHSTEIN SI Y ROBINSON SK (eds) Parasiticbirds and their hosts: studies in coevolution. OxfordUniversity Press, Oxford
SCHLUTER D, PRICE T, MOORES AO Y LUDWIG D (1997)Likelihood of ancestor state in adaptative radiation.Evolution 51:1649–1711
SEALY G Y NEUDORF DL (1995) Male northern orioleseject cowbird eggs: implications for the evolutionof rejection behavior. Condor 97:369–375
SEALY G, NEUDORF DL Y HILL DP (1995) Rapid layingby brown-headed cowbirds Molothrus ater and otherparasitic birds. Ibis 137:76–84
SMITH NG (1968) The advantage of being parasitized.Nature 219:690–694
STRAUSBERGER BM (1998) Temperature, egg mass,and incubation time: a comparison of brown-headed cowbirds and red-winged blackbirds.Auk 115:863–850
WEATHERHEAD PJ (1991) The adaptive value of thick-shelled eggs for brown-headed cowbirds. Auk108:196–198
ZAR JH (1996) Biostatistical analysis. Tercera edición.Prentice Hall, Upper Saddle River

How to cite

E. Manuela Pujol , Myriam E. Mermoz (2006). Reconstruction of ancestral states of life-history traits in cowbirds: an analysis of adaptations to brood parasitism. El Hornero, Vol. 21 No. 1 (2006), 15-23. https://doi.org/10.56178/eh.v21i1.794

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[1] ARAGÓN S, MOLLER AP, SOLER JJ Y SOLER M (1999)Molecular phylogeny of cuckoos supports a poly-phyletic origin of brood parasitism. Journal of Evolu-tionary Biology 12:495–506

[2] BJÖRKLUND M (1997) Are “comparative methods” al-ways necessary? Oikos 80:607–612

[3] BROOKER LC Y BROOKER MG (1991) Eggshell strengthin cuckoos and cowbirds. Ibis 133:406–413

[4] CADENA CD, CUERVO AM Y LANYON SM (2004) Phy-logenetic relationships of the red-bellied grackle(Icteridae: Hyppyrrhus pyrohypogaster) inferredfrom mitochondrial DNA sequence data. Condor106:664–671

[5] CARTER MD (1986) The parasitic behavior of thebronzed cowbird in south Texas. Condor 88:11–25

[6] CLAYTON NS, REBOREDA JC Y KACELNIK A (1997) Sea-sonal change of hippocampus volume in parasiticcowbirds. Behavioral Processes 41:237–243

[7] DAVIES NB (2000) Cuckoo, cowbirds and other cheats.Academic Press, Londres

[8] DAVIES NB Y BROOKE LC (1989) An experimental studyof co-evolution between the cuckoo, Cuculus canarusand its host. II. Host egg markings, chick discrimi-nation and general discussion. Journal of AnimalEcology 58:225–236

[9] FELSENSTEIN J (1985) Phylogenies and the compara-tive data. American Naturalist 125:1–15

[10] FRAGA RM (1998) Interactions of the parasitic scream-ing and shiny cowbirds (Molothrus rufoaxillaris andM. bonariensis) with a shared host, the bay-wingedcowbird (Molothrus badius). Pp. 173–193 en:ROTHSTEIN SI Y ROBINSON SK (eds) Parasitic birds andtheir hosts: studies in coevolution. Oxford UniversityPress, Nueva York

[11] FRAGA RM Y DI GIACOMO A (2004) Cooperative breed-ing of the yellow-rumped marshbird (Icteridae) inArgentina and Paraguay. Condor 106:671–673

[12] FRIEDMANN H (1929) The cowbirds, a study in the biologyof the social parasitism. CC Thomas, Springfield

[13] FRIEDMANN H (1960) The parasitic weaverbirds. UnitedStates National Museum Bulletin 223:1–196

[14] GARLAND JR T Y ADOLPH SC (1994) Why not to do twospecies comparative studies: limitations on inferringadaptations. Physiological Zoology 67:797–828

[15] GARLAND JR T, BENNETT A Y REZENDE EL (2005) Phylo-genetic approaches in comparative physiology.Journal of Experimental Biology 208:3015–3035

[16] GARLAND JR T E IVES AR (2000) Using the past to pre-dict the present: confidence intervals for regressionequation in phylogenetic comparative methods.American Naturalist 155:346–364

[17] GARLAND JR T, MARTIN KML Y DÍAZ-URIARTE R (1997)Reconstructing ancestral trait values using squared-change parsimony: plasma osmolarity at the originof amniotes. Pp. 425–501 en: SUMIDA SS y MARTINKLM (eds) Amniote origins: completing the transitionto land. Academic Press, San Diego

[18] GARLAND JR T, MIDFORD PE E IVES AR (1999) An intro-duction to phylogenetically based statistical meth-ods, with a new method for confidence intervalson ancestral states. American Zoology 39:374–388

[19] GOULD SJ Y VBRA ES (1982) Exaptation —a missingterm in the science of form. Paleobiology 8:4–15

[20] GRIM T (2005) Mimicry vs. similarity: which resem-blances between brood parasites and their hosts aremimetic and which are not? Biological Journal of theLinnean Society 84:69–78

[21] HUDSON WH (1874) Notes on the procreant instinctsof the three species of Molothrus found in BuenosAyres. Proceedings of the Zoological Society of London9:153–174

[22] JOHNSON KP Y LANYON SM (1999) Molecular system-atics of the grackles and allies, and effect of addi-tional sequence (Cyt b and ND2). Auk 116:759–768

[23] KATTAN GH (1995) Mechanism of short incubationperiod in brood parasitic cowbirds. Auk 112:335–342

[24] KATTAN GH (1996) Growth and provisioning of shinycowbirds and house wren host nestling. Journal ofField Ornithology 67:434–441

[25] LANYON SM (1992) Interspecific brood parasitism inblackbirds (Icterinae): a phylogenetic perspective.Science 225:77–79

[26] MADDISON WP (1991) Squared-changed parsimonyreconstruction of ancestral states for continuous-valued character on a phylogenetic tree. SystematicZoology 40:304–314

[27] MARTINS EP (1999) Estimation of ancestral states ofcontinuous character: a computer simulation study.Systematic Biology 48:642–650

[28] MARTINS EP Y GARLAND JR T (1991) Phylogenetic analy-ses of the correlated evolution of continuous char-acter: a simulation study. Evolution 45:534–557

[29] MASON P (1986) Brood parasitism in a host general-ist, the Shiny Cowbird: I. The quality of differentspecies as hosts. Auk 103:52–60

[30] MERMOZ ME (1996) Interacciones entre el tordo renegri-do Molothrus bonariensis y el pecho amarillo Pseudoleistesvirescens: estrategias del parásito de cría y mecanismosde defensa del hospedador. Tesis doctoral, Universidadde Buenos Aires, Buenos Aires

[31] MERMOZ ME Y ORNELAS JF (2004) Phylogenetic analy-sis of life-history adaptations in parasitic cowbirds.Behavioral Ecology 15:109–119

[32] MERMOZ ME Y REBOREDA JC (1999) Egg layingbehaviour by shiny cowbirds parasitizing brown-and-yellow marshbirds. Animal Behaviour 58:873–882

[33] OAKLEY TH Y CUNNINGHAM CW (2000) Independent con-trasts succeed where ancestor reconstruction fails inknown bacteriophage phylogeny. Evolution 54:397–405

[34] ORTEGA CP Y CRUZ A (1992) Differential growth pat-terns of nestling brown-headed cowbirds and yel-low-headed blackbirds. Auk 109:368–376

[35] PAYNE RB (1973) Individual laying histories and theclutch size and numbers of eggs of parasitic cuck-oos. Condor 75:414–438

[36] PAYNE RB (1977) The ecology of brood parasitism inbirds. Annual Review of Ecology and Systematics 8:1–28

[37] PAYNE RB, PAYNE LL Y WOODS JL (2000) Imprintingand the origin of parasite-host species associationsin brood-parasitic indigobirds, Vidua chalybeata.Animal Behaviour 59:69–81

[38] PUJOL EM (2005) Evolución de las características dehistoria de vida en el grupo que dio origen a los tordosparásitos (Aves: Icteridae). Tesis de Licenciatura, Uni-versidad de Buenos Aires, Buenos Aires

[39] RAHN H, CURRAN-EVERET L Y BOOTH DT (1988) Egg-shell differences between parasitic and nonparasiticIcteridae. Condor 90:962–964REEVE HK Y SHERMAN PW (1993) Adaptation and thegoals of evolutionary research. Quarterly Review ofBiology 68:1–31

[40] REZENDE EL Y GARLANDJR T (2003) Comparacionesinterespecíficas y métodos estadísticos filogenéticos.Pp. 79–98 en: BOZINOVIC F (ed) Fisiología ecológica yevolutiva. Teoría y casos de estudio en animales. Edicio-nes Universidad Católica de Chile, Santiago

[41] ROHWER S Y SPA W CD (1988) Evolutionary lag versusbill-size constraints: a comparative study of theacceptance of cowbirds eggs by old hosts. Evolution-ary Ecology 2:27–36

[42] ROTHSTEIN SI (1990) A model system for coevolution:avian brood parasitism. Annual Review of Ecology andSystematics 21:481–508

[43] ROTHSTEIN SI Y ROBINSON SK (1998) The evolution andecology of avian brood parasitism: an overview. Pp.3–58 en: ROTHSTEIN SI Y ROBINSON SK (eds) Parasiticbirds and their hosts: studies in coevolution. OxfordUniversity Press, Oxford

[44] SCHLUTER D, PRICE T, MOORES AO Y LUDWIG D (1997)Likelihood of ancestor state in adaptative radiation.Evolution 51:1649–1711

[45] SEALY G Y NEUDORF DL (1995) Male northern orioleseject cowbird eggs: implications for the evolutionof rejection behavior. Condor 97:369–375

[46] SEALY G, NEUDORF DL Y HILL DP (1995) Rapid layingby brown-headed cowbirds Molothrus ater and otherparasitic birds. Ibis 137:76–84

[47] SMITH NG (1968) The advantage of being parasitized.Nature 219:690–694

[48] STRAUSBERGER BM (1998) Temperature, egg mass,and incubation time: a comparison of brown-headed cowbirds and red-winged blackbirds.Auk 115:863–850

[49] WEATHERHEAD PJ (1991) The adaptive value of thick-shelled eggs for brown-headed cowbirds. Auk108:196–198

[50] ZAR JH (1996) Biostatistical analysis. Tercera edición.Prentice Hall, Upper Saddle River