Clinal variation in the polymorphic Black Sparrowhawk Accipiter melanoleucus is unrelated to infection by the blood parasite Haemoproteus nisi

Abstract

Blood parasites can impact host fitness and can, thus, act as selective agents in their host’s evolution. The melanocortin system linked to colouration of vertebrates may infer higher parasite resistance via pleiotropic properties of the genes involved. Black Sparrowhawks (Accipiter melanoleucus) are colour polymorphic (dark and light morph adults) and distributed clinally in South Africa, with more dark morphs in the Southwest where the breeding season coincides with the rainy season. There, dark morphs have lower infections of haemosporidian parasites Haemoproteus nisi, suggesting a higher parasitic resistance. Thus, it is hypothesized that the morph distribution may be an adaptive response to coping with varying parasite prevalence associated with rainfall levels, which may regulate the parasites’ invertebrate vectors. This hypothesis assumes a fitness cost of high parasite burden, which could be specifically important during the energy-demanding breeding season. To explore this, we (1) quantified Black Sparrowhawk H. nisi infections across South Africa, and explored (2) breeding performance and apparent annual survival of adults, and (3) nestling body condition in Cape Town in relation to infection levels. In contrast to the predictions, we found that parasite prevalence did not vary across the country, we found no fitness costs of higher infection levels for breeding birds, and also nestling body condition was independent of infection levels. Thus, we found no support for our hypothesis. Black Sparrowhawk polymorphism is unlikely to be driven by an adaptive function linked to dealing with higher infections with H. nisi in regions with wetter breeding seasons.

Zusammenfassung

Klinale Veränderungen der Gefiederfärbung von Dominohabichten Accipiter melanoleucus sind unabhängig von der Infektion mit dem Blutparasiten Haemoproteus nisi.

Blutparasiten können die Fitness ihrer Wirte beeinflussen und sind so Teil der natürlichen Selektion in der Wirtsevolution. Das Melanocortin System, welches in Wirbeltieren in Zusammenhang mit der Färbung steht, kann via pleiotroper Effekte der beteiligten Gene eine höhere Resistenz gegen Parasiten vermitteln. Dominohabichte (Accipiter melanoleucus) weisen einen Farbpolymorphismus auf, wobei die dunklen Morphen vor allem im Südwesten von Südafrika vorkommen, und die hellen Morphen vor allem im Nordosten. Sie folgen einer klinalen Variation entsprechend variierender Niederschlagsmengen während der Brutsaison. Im Raum Kapstadt, wo die Brutsaison mit der Regenzeit zusammenfällt, zeigen dunkle Morphen niedrigere Infektionen mit dem Blutparasiten Haemoproteus nisi, was auf eine Resistenz gegen den Parasiten hindeutet. Eine gängige Hypothese in solch polymorphen System ist, dass Niederschlagsmengen das Vorkommen der Vektoren, welche Blutparasiten übertragen, regeln, und so indirekt die Verbreitung der verschiedenen Morphen in einer Population beeinflussen. Diese Hypothese sagt Fitnesskosten hoher Parasiteninfektionen voraus, die vor allem in der energieaufwändigen Brutsaison maßgeblich sein könnten. In dieser Studie verschneiden wir die Haemoproteus nisi Infektion von Dominohabichten mit i) der Verbreitung der Morphen in Südafrika; ii) dem Bruterfolg und den Überlebensraten von Altvögeln; sowie, iii) der Körperkondition der Küken einer Population in Kapstadt. Wider Erwarten variieren die Infektionsraten nicht entsprechend des geografischen Gradienten der relativen Häufigkeiten beider Morphen im südafrikanischen Verbreitungsgebiet, noch wurden negative Fitesskonsequenzen der Parasitenbelastung in Hinblick auf Bruterfolg und Körperkondition festgestellt. Es ist daher sehr unwahrscheinlich, dass der Farbpolymorphismus von Dominohabichten eine Adaption an höhere Infektionen mit Haemoproteus nisi in regenreichen Regionen ist.

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Availability of data

The dataset will be available as electronic material on UCT’s ZivaHub; the according DOI code will be provided upon acceptance of the manuscript for publication.

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Acknowledgements

We are grateful to the Black Sparrowhawk Team—Johan Koeslag, Mark Cowen, Odette Curtis, Margaret MacIver, Sharon Pryce, Jessleena Suri, Shane McPherson and Carina Nebel—for the long-term population monitoring, data collection and extensive support in the field. We wish to thank Gabriella Leighton, Michelle Maritz, Jessleena Suri, Bonnie Lei and Elelwani Musekwa for their assistance in analysing blood slides. We are very grateful to all the landowners who permitted us to conduct fieldwork on their land and particularly to the South African National Parks (SANPARKS) for access to the Table Mountain National Park.

Funding

The Black Sparrowhawk Project is funded by the DST-NRF Centre of Excellence and a South Africa (NRF)/Sweden (STINT) science and technology research collaboration (Grant no.: STINT 160909188048). PS was supported by the Claude Leon Foundation post-doctoral fellowship and the Leslie Brown Memorial Grant of the Raptor Research Foundation.

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The idea for this study originally came from AA and PS. Data were collected by AK, GT and PS. Help by others is accordingly acknowledged. The statistical analyses were performed by SM, GT and PS. The manuscript was prepared by SM, AA and PS, with edits provided by GT. Volunteers, field and lab assistants have been accredited accordingly.

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Correspondence to Samantha McCarren.

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Ethical clearance was obtained for all procedures required for the long-term study on the Cape Peninsula and for adult trapping across South Africa in 2014. The research was approved by the University of Cape Town’s Science Faculty Animal Ethics Committee (permit number: 2012/V37/AA; 2016/v11/AA), and was in line with South African legal requirements. All necessary permits for monitoring, capturing and ringing birds were acquired from Cape Nature and South African National Parks (SANPARKS).

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McCarren, S., Sumasgutner, P., Tate, G. et al. Clinal variation in the polymorphic Black Sparrowhawk Accipiter melanoleucus is unrelated to infection by the blood parasite Haemoproteus nisi. J Ornithol (2020). https://doi.org/10.1007/s10336-020-01823-3

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Keywords

  • Raptor
  • Polymorphism
  • Haemosporidian parasites
  • Avian malaria
  • Melanin
  • Pleiotropy