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Male parental effort predicts reproductive contribution in the joint-nesting, Smooth-billed Ani (Crotophaga ani)

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Abstract

Co-operative breeders provide parental care to non-filial offspring—a behaviour known as ‘alloparental care’. While inclusive fitness benefits are a widely accepted driver of alloparental care in kin-based social groups, such indirect benefits are lost in non-kin societies. Among such societies, theory predicts that the degree of parental and alloparental effort should therefore be proportional to an individual’s genetic contribution to mixed broods—depending upon reproductive options. Using genotyping data across five to 12 microsatellite loci for individuals from 20 social groups (67 adults and 153 nestlings), we assessed whether kinship or proportional reproductive success explained trends in parental and alloparental effort in the Smooth-billed Ani (Crotophaga ani), a joint-nesting cuckoo species. Nocturnal incubation in this species appears to be performed almost exclusively by a single male. We first report significantly higher degrees of relatedness between adults within social groups (\(\bar{r}\) = 0.208, n = 114 dyads), than between social groups (\(\bar{r}\) = 0.120, n = 893 dyads), suggesting that inclusive fitness benefits may in part explain uneven allocation of parental effort. Second, we show that nocturnal incubation status is a significant predictor of reproductive success in males, as nocturnal incubators sire a greater proportion of nestlings in mixed-parentage broods. While patterns of reproductive skew appear high at 80% paternal confidence (\(\bar{B}\) = 0.052, p = 0.061), we report no significant deviation from an egalitarian breeding framework. Our results revealed similar patterns of reproductive allocation to closely related Groove-billed Anis (Crotophaga sulcirostris); however, differences in male reproductive skew and within-group relatedness across crotophagids are highlighted and offer insight into social evolution among anis.

Zusammenfassung

Der väterliche Aufwand bei der Brutfürsorge liefert Voraussagen zum reproduktiven Beitrag beim gemeinschaftlich nistenden Glattschnabelani ( Crotophaga ani )

Bruthelfer wenden elterliche Fürsorge für anderen als den eigenen Nachwuchs auf—dieses Verhalten ist auch als alloparentale Fürsorge bekannt. Während dadurch bedingte Vorteile für die Fitness weithin als Treibkraft für nicht-elterliche Fürsorge in verwandtschaftsbasierten sozialen Gruppen gelten, verlieren sich solche indirekten Vorteile in nicht verwandtschaftsbasierten Gruppen. Es ist daher theoretisch zu erwarten, dass das Ausmaß elterlichen beziehungsweise nicht-elterlichen Aufwands in solchen Gruppen proportional zum eigenen genetischen Beitrag zu den gemischten Bruten stehen sollte—abhängig von den reproduktiven Möglichkeiten. Anhand genotypischer Daten für 5–12 Mikrosatelliten-Loci von Individuen aus 20 sozialen Gruppen (67 Altvögel und 153 Nestlinge) prüften wir, ob Verwandtschaft oder proportionaler Bruterfolg Trends im elterlichen beziehungsweise nicht-elterlichen Fürsorgeaufwand beim Glattschnabelani (Crotophaga ani), einer gemeinschaftlich nistenden Kuckucksart, erklären konnten. Bei dieser Art scheint die Bebrütung bei Nacht fast ausschließlich durch ein einzelnes Männchen zu erfolgen. Zunächst stellten wir signifikant höhere Verwandtschaftsgrade zwischen Altvögeln innerhalb der sozialen Gruppen (r = 0208; n = 114 Dyaden) als zwischen den Gruppen (r = 0120, n = 893 Dyaden) fest, was darauf hindeutet, dass Vorteile für die Fitness die ungleiche Verteilung elterlicher Fürsorge zum Teil erklären können. Zweitens konnten wir zeigen, dass der Brutstatus bei Nacht ein signifikanter Voraussagewert für den Reproduktionserfolg der Männchen ist, insofern, als dass Männchen, welche nachts auf dem Nest sitzen, einen größeren Anteil Nestlinge in Bruten gemischter Herkunft zeugen. Während die Ungleichverteilung bei der Fortpflanzung mit 80% väterlicher Konfidenz hoch erscheint (B = 0, 052; p = 0061), können wir keine signifikante Abweichung von einem egalitären Brutsystem feststellen. Die von uns ermittelten Muster der Anteile an der Fortpflanzung ähneln denen beim nahe verwandten Riefenschnabelani (Crotophaga sulcirostris), allerdings beleuchten wir auch Unterschiede in der Schiefe bei der Reproduktion der Männchen sowie dem Verwandtschaftsgrad innerhalb der Gattung Crotophaga und geben einen Einblick in die soziale Evolution der Anis.

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Acknowledgements

We would like to thank Oscar Diaz, Susan Silander, James Padilla and surrounding staff at the Cabo Rojo National Wildlife Refuge, F. Ramos, Dr V. Sánchez, A. Franqui and M. Toro of Finca Altamira for providing open access to their land. Thank you to L. Barabas, M. Beaucreux, A. Bjärhall, A. Boon, B. Bravery, M. Cruz, H. Darrow, A. Demko, J. Eyster, L. Froese, J. Haselmayer, J. S. Hing, H. Kuo, R. Land, K. Peiman, T. Pope, H. Reider, N. Roach, E. I. Rodriguez, Rutherford, S. Schopman, K. Stein, F. Tarazona, S. Turner, B. M. Wadien, S. Wheeler, for support in sample collection and Drs Jonathon Dushoff and Ben Bolker for statistical advice. All animal handling and sampling was approved by the McMaster University Animal Care Committee and conducted according to a McMaster University Animal Utilization Permit (AUP 13-10-37).

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Authors and Affiliations

  1. Department of Biology, McMaster University, 1280 Main Street West, Hamilton, ON, L8S 4K1, Canada

    Joshua K. Robertson, John R. Caldwell, Leanne A. Grieves, Annika Samuelsen, Gregory S. Schmaltz & James S. Quinn

  2. Department of Biology, University of McGill, 1205 Avenue du Docteur-Penfield, Montreal, QC, H3A 1B1, Canada

    John R. Caldwell

  3. Department of Biology, University of Western Ontario, 1151 Richmond St, London, ON, N6A 3K7, Canada

    Leanne A. Grieves

  4. Department of Biology, Abbotsford Campus, University of the Fraser Valley, 33844 King Road, Abbotsford, BC, V2S 7M7, Canada

    Gregory S. Schmaltz

  5. Department of Biology, Trent University, 1600 West Bank Drive, Peterborough, ON, K9L OG2, Canada

    Joshua K. Robertson

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Correspondence to Joshua K. Robertson.

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This research was supported by a Natural Science and Engineering Research Council Grant to J. S. Q. and a Queen Elizabeth II Graduate Scholarship (Government of Ontario) to J. K. R. Additional funding was provided by the Wilson Ornithological Society to J. K. R.

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Communicated by C. G. Guglielmo.

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Robertson, J.K., Caldwell, J.R., Grieves, L.A. et al. Male parental effort predicts reproductive contribution in the joint-nesting, Smooth-billed Ani (Crotophaga ani). J Ornithol 159, 471–481 (2018). https://doi.org/10.1007/s10336-017-1522-z

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