Female chickadees living in monogamous mating systems will proactively seek out males that have better cognitive skills than their nestmate, according to new findings.
The research, published today as a Reviewed Preprint in eLife, is described by the editors as an important study using robust genetic analyses and experimental design, providing compelling evidence that females seeking out extra-pair copulations prefer males with strong spatial cognition, and that these males have a reproductive advantage over other males.
Across animal species, females commonly mate with more than one male, even in monogamous mating systems. These so-called extra-pair copulations can increase the fitness of offspring via several mechanisms, including genetic benefits. Understanding the factors that influence choice of mate and the consequences of these decisions on survival and fitness is a central focus of evolutionary biology research.
"When it comes to selecting a mate, females tend to be the 'choosier' sex due to their inherent investment. Females seek 'high-quality' males to increase the likelihood of successful reproduction, good parental care, and the chance that their offspring inherit 'good' genes," says lead author Carrie Branch, Assistant Professor at Western University, Ontario, Canada. "Cognitive abilities such as spatial learning and memory allow animals to succeed in variable environments and can be directly inherited and shaped by natural selection, but there is little evidence to show that females choose males with better cognitive abilities."
To address this, the team followed a population of wild North American mountain chickadees: socially monogamous, non-migratory birds that rely on specialized spatial cognition to recover food stores. They used 'smart' feeder arrays – programmed so that only one location per chickadee would result in a rewarding sunflower seed – to assess individual spatial cognition. The more errors a chickadee made in relocating the food source, the lower their cognitive ability. Alongside this, the team quantified extra-pair paternity over three breeding seasons and compared the spatial cognition skills of the extra-pair males with those of the social male they cuckolded.
Across the three-year study, around a third of the offspring sampled were sired by extra-pair males and 70% of nests had at least one chick resulting from extra-pair copulation (extra-pair young). The researchers found that males with better spatial learning and memory abilities (fewer location errors in the food recovery trials) sired more extra-pair young. In fact, those males that performed best in the cognition tests may sire between six and seven extra-pair young a year, and the age of the males had no bearing on the number of extra-pair young they sired.
The team next looked at the reproductive fitness of the males and how this related to their spatial cognition skills. Males that sired extra-pair young did not appear to lose any reproductive fitness in their own nests, as there was no difference in the number of chicks or chick mass between the extra-pair males and the social males – although males with better spatial cognition raised heavier young overall.
Importantly, as the team hypothesised, extra-pair males had better spatial learning and memory abilities than the social males they cuckolded, even though there was no significant difference in age. This finding suggests that females may preferentially mate with males that have better spatial cognition than their social mate.
However, the likelihood of being cuckolded was not directly related to the social male's cognitive skills. Instead, females that performed worse in the cognitive tests were more likely to have extra-pair young in their nests, suggesting that females might also seek males in response to their own cognitive deficiencies.
"Our results show that female choice contributes to the evolution of spatial cognitive abilities in a species that stores and recovers thousands of food items and relies on spatial cognition for survival," concludes senior author Vladimir Pravosudov, Professor of Biology at the University of Nevada, Reno, US. "Males with better spatial cognition sired more young and fledged heavier chicks, which are more likely to survive and enter the breeding population. Our findings add to the evidence supporting natural selection based on spatial cognitive abilities in wild chickadees."
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