American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

“Understanding the social dynamics of breeding phenology: indirect genetic effects and assortative mating in a long distance migrant”

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Maria Moiron, Yimen G. Araya-Ajoy, Céline Teplitsky, Sandra Bouwhuis, and Anne Charmantier (Nov 2020)

Breeding timing is influenced by indirect partner effects and assortative mating for migratory phenotype of pair members

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The timing of female breeding is influenced by males and assortative mating for migratory phenotype in common terns

Pair of common terns (<i>Sterna hirundo</i>) from the long-term study population at the Banter See on the German North Sea coast.<br/>(Credit: Sandra Bouwhuis).<br/>
Pair of common terns (Sterna hirundo) from the long-term study population at the Banter See on the German North Sea coast.
(Credit: Sandra Bouwhuis).

The date at which the first egg of a clutch is laid is a trait expressed exclusively by female birds. Yet males and females interact and, as a result, males might also influence when their partners will start laying eggs. For instance, males of various species provide food as part of courtship feeding events that reinforce the pair bond, and more or better food may lead to earlier laying.

From an evolutionary point of view, it is not only important to investigate whether male effects on female traits exist, but also whether they are underpinned by a genetic component, because, if so, they may facilitate or constrain evolutionary responses to selection.

Researchers from the Centre d’Écologie Fonctionnelle et Évolutive (France), Institute of Avian Research (Germany), and Norwegian University of Science and Technology (Norway) investigated male effects on female egg laying date using data from a population of individually marked common terns studied during their breeding seasons in Germany for over 30 years. Common terns are migratory seabirds and the ones breeding in Germany spend their winters in West Africa, arrive at the breeding colony in April-May, and start breeding in May-June.

The team found that males influence female laying date, and this effect has a genetic component. Further analyses revealed that male arrival date was a trait underlying the observed male effect, and that it may largely be explained by assortative mating for arrival date: males that consistently arrive early mate with females that consistently arrive early and birds that arrive early also lay early. Moiron and colleagues therefore argue that it is not only important to study partner effects, but to also uncover the potential causal pathways and confounding effects underlying them.

 

El inicio de la reproducción en las hembras de charrán común está influenciado por los machos y el apareamiento selectivo acorde al fenotipo migratorio

La fecha del primer huevo de una nidada es un rasgo expresado exclusivamente por las hembras. Sin embargo, machos y hembras interactúan y, como resultado, los machos también pueden influir en el inicio de la puesta de huevos. Por ejemplo, los machos de varias especies proporcionan alimentos durante el cortejo. Este cortejo sirve para reforzar el vínculo de pareja, y a la vez, al proporcionar más o mejor comida, puede repercutir en una puesta más temprana.

Desde un punto de vista evolutivo, no solo es importante investigar si existe un efecto del macho en los rasgos de la hembra, sino también si estos tienen un componente genético, ya que, de ser así, pueden facilitar o restringir las respuestas evolutivas a la selección.

Investigadores del Centre d’Écologie Fonctionnelle et Évolutive (Francia), el Institute of Avian Research (Alemania) y la Norwegian University of Science and Technology (Noruega) han estudiado los efectos que el macho puede inducir en la fecha de puesta de huevos de la hembra utilizando datos de una población de charranes comunes marcados individualmente, y que han sido estudiados durante sus temporadas de cría en Alemania durante más de 30 años. Los charranes comunes son aves marinas migratorias y los que se reproducen en Alemania pasan sus inviernos en África occidental, llegan a la colonia reproductora en abril-mayo y comienzan a reproducirse en mayo-junio.

El equipo de investigadores descubrió que los machos influyen en la fecha de puesta de las hembras, y que este efecto tiene un componente genético. Análisis adicionales revelaron que la fecha de llegada de la migración del macho era un rasgo subyacente al efecto del macho observado, y que puede explicarse en gran medida por el apareamiento selectivo acorde con la fecha de llegada de migración. Moiron y sus colaboradores, por lo tanto, argumentan que no solo es importante estudiar los efectos de pareja en la puesta de huevos, sino también descubrir las posibles vías causales y la existencia de sesgos subyacentes.


Abstract

Phenological traits, such as the timing of reproduction, are often influenced by social interactions between paired individuals. Such partner effects may occur when pair members affect each other’s pre-breeding environment. Partner effects can be environmentally and/or genetically determined, and quantifying direct and indirect genetic effects is important for understanding the evolutionary dynamics of phenological traits. Here, using 26 years of data from a pedigreed population of a migratory seabird, the common tern (Sterna hirundo), we investigate male and female effects on female laying date. We find that female laying date harbors both genetic and environmental variation, and is additionally influenced by the environmental, and, to a lower extent, genetic, component of its mate. We demonstrate this partner effect to be largely explained by male arrival date. Interestingly, analyses of mating patterns with respect to arrival date show mating to be strongly assortative and, using simulations, we show that assortative mating leads to overestimation of partner effects. Our study provides evidence for partner effects on breeding phenology in a long distance migrant, while uncovering the potential causal pathways underlying the observed effects and raising awareness for confounding effects due to assortative mating or other common environmental effects.