Sublethal effects of natural parasitism act through maternal, but not paternal, reproductive success in a wild population

Abstract

Parasites are a major component of all animal populations. Males and females often differ in their levels of parasite prevalence, potentially leading to sex differences in the impact of parasitism on fitness, with important implications for the evolution of parasite and host traits including resistance, tolerance, and virulence. However, quantitative measures of the impact of parasitism under free-living conditions are extremely rare, as they require detailed host demographic data with measures of parasite burden over time. Here, we use endoscopy for direct quantification of natural-parasite burdens and relate these to reproductive success over 7 yr in a wild population of seabirds. Contrary to predictions, only female burdens were associated with negative impacts of parasitism on breeding success, despite males having significantly higher burdens. Female reproductive success declined by 30% across the range of natural parasite burdens. These effects persisted when accounting for interannual population differences in breeding success. Our results provide quantitative estimates of profound sublethal effects of parasitism on the population. Importantly, they highlight how parasites act unpredictably to shape ecological and evolutionary processes in different components of the same population, with implications for demography and selection on host and parasite traits.

Interactions between Environmental Contaminants and Gastrointestinal Parasites: Novel Insights from an Integrative Approach in a Marine Predator

“…Little is known on the drivers of parasite prevalence and loads in free-ranging birds. 3 , 14 , 77 As predicted by testosterone-induced immunosuppression 11 and in agreement with previous results, 29 males had higher C. rudolphii loads than females ( Table 1 ). Feeding habitat (δ 13 C Bulk ) and trophic position (corr-δ 15 N Bulk ) were not related to C. rudolphii loads in either sex ( Figure S6 and Table S8 ).…”

“…After blood sampling, we used endoscopy to quantify the load of gastrointestinal worms in a nondestructive manner in all birds. An endoscope (103 cm long, 9 mm diameter) was gently inserted into the esophagus and stomach, and worms were counted visually using the endoscope’s camera images (details in Burthe et al 28 and Hicks et al 29 ). All videos were recorded for further count verifications.…”

“… 28 Shags have variable burdens of the nematode Contracaecum rudolphii that negatively impacts adults and nestlings. 4 , 29 Shags become infected via their fish diet, but drivers of between-individual differences in parasite loads are poorly understood. 30 Sex differences in parasite loads and their fitness effects have been reported previously, 29 and sexual size dimorphism is likely to influence shag foraging strategies.…”

“…At the focal study site, shags are of known sex, age, and breeding history and can be monitored nondestructively for the presence of gastrointestinal parasites through endoscopy . Shags have variable burdens of the nematode Contracaecum rudolphii that negatively impacts adults and nestlings. , Shags become infected via their fish diet, but drivers of between-individual differences in parasite loads are poorly understood . Sex differences in parasite loads and their fitness effects have been reported previously, and sexual size dimorphism is likely to influence shag foraging strategies. , Therefore, this is a unique system to address critical gaps in the understanding of how intrinsic and extrinsic factors determine individual contaminant and parasite loads and their interactions.…”

“…Shags have variable burdens of the nematode Contracaecum rudolphii that negatively impacts adults and nestlings. , Shags become infected via their fish diet, but drivers of between-individual differences in parasite loads are poorly understood . Sex differences in parasite loads and their fitness effects have been reported previously, and sexual size dimorphism is likely to influence shag foraging strategies. , Therefore, this is a unique system to address critical gaps in the understanding of how intrinsic and extrinsic factors determine individual contaminant and parasite loads and their interactions.…”