Pleiotropic effects of melanin pigmentation: haemoparasite infection intensity but not telomere length is associated with plumage morph in black sparrowhawks

Abstract

There is increasing recognition of the potential pleiotropic effects of melanin pigmentation, particularly on immunity, with reports of variation in haemoparasite infection intensity and immune responses between the morphs of colour-polymorphic bird species. In a population of the black sparrowhawk (Accipiter melanoleucus) in western South Africa, light morphs have a higher haemoparasite infection intensity, but no physiological effects of this are apparent. Here, we investigate the possible effects of haemoparasite infection on telomere length in this species and explore whether relative telomere length is associated with either plumage morph or sex. Using quantitative polymerase chain reaction analysis, we confirmed that dark morphs had a lower haemoparasite infection intensity than light morphs. However, we found no differences in telomere length associated with either the haemoparasite infection status or morph in adults, although males have longer telomeres than females. While differences in haemoparasite intensity between morphs are consistent with pleiotropic effects of melanin pigmentation in the black sparrowhawk, we found no evidence that telomere length was associated with haemoparasite infection. Further work is needed to investigate the implications of possible pleiotropic effects of plumage morph and their potential role in the maintenance of colour polymorphism in this species.

Keywords: Accipiter; haemoparasite; melanin; pleiotropy; polymorphism; telomere.

Figure 1.

Relationship between haemoparasite infection intensity as determined by microscopy and qPCR in adult black sparrowhawks. Haemoparasite infection intensity determined by microscopy (number of cells infected by Haemoproteus or Leucocytozoon per 10 000 erythrocytes) is significantly positively correlated with that determined by qPCR (R ² = 0.98, F _1,66 = 3826 and p < 0.001). The main figure excludes all samples for which the haemoparasite intensity estimated by microscopy is greater than 10 to better visualize the relationship. (Inset: full figure, including all samples. n = 68).

Figure 2.

Box plot showing the natural logarithm of haemoparasite infection intensity (determined by qPCR) in dark and light morph adult black sparrowhawks. Light morph birds have significantly higher haemoparasite infection intensity than dark morph individuals (F _1,62 = 12.48 and p < 0.001). Boxes show the median and interquartile range, while the upper and lower whiskers extend to the highest or lowest value within 1.5 times the interquartile range. n = 64.

Figure 3.

Relative telomere length (determined by qPCR) of black sparrowhawks as nestlings versus adults. The age at which individuals were resampled is shown on the x-axis. Lines connect the same individuals sampled at two different points in time. Adults have significantly shorter telomeres than nestlings (χ ² _{1, 24} = 32.47 and p < 0.001). Sex of the individuals is indicated by colours (blue = female and red = male). n = 12.

Figure 4.

Relationship between the relative telomere length (determined by qPCR) and the natural logarithm of the haemoparasite infection intensity (determined by qPCR) in infected adult black sparrowhawks. The haemoparasite infection intensity was not significantly associated with relative telomere length (F _1,62 = 0.02, p = 0.89). n = 64.

Figure 5.

Relative telomere length (determined by qPCR) in adult female black sparrowhawks versus males. The difference between the sexes was significant, with males having longer telomeres than females (F _1,87 = 6.73 and p = 0.011). The boxes show the median and interquartile range, while the upper and lower whiskers extend to the highest or lowest value within 1.5 times the interquartile range. n = 89.

Figure 6.

Relationship between the relative telomere length (determined by qPCR) and the condition index in adult black sparrowhawks. Sex of the individuals is indicated by point shapes. Relative telomere length is significantly negatively associated with the condition index (F _1,64 = 5.32 and p = 0.024). n = 69.