“Rapid divergence of predator functional traits affects prey composition in aquatic communities”

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Dominik W. Schmid, Matthew D. McGee, Rebecca J. Best, Ole Seehausen, and Blake Matthews (Mar 2019)

The DOI will be https://dx.doi.org/10.1086/701784

Rapid trait evolution in recently diverged predator populations impacts predator performance and prey community structure

Morphological and performance analysis reveals key foraging traits in young and rapidly diverging predator populations

The author Dominik W. Schmid peering at threespine stickleback (Gasterosteus aculeatus) from Lake Constance, Switzerland.
(Credit: Michael Schreiber)

Darwin was the first to identify that variation in traits amongst individuals is the basis upon which selection can act. But interestingly, trait functionality is often assumed rather than tested empirically (i.e. longer legs equals faster running). Yet many functions, such as prey pursue, capture, and ingestion, require many traits to interact. This makes it difficult to disentangle which traits are key to a specific function. In this paper Dominik W. Schmid, Matt McGee, Rebecca J. Best, Ole Seehausen, and Blake Matthews at EAWAG (Switzerland) have specifically looked into the trait utility (i.e. fitness advantage of traits in a given environmental context) of a predator’s foraging morphology and its consequences for prey capture and community structure.

The marine ancestors of threespine stickleback (Gasterosteus aculeatus) repeatedly and independently invaded freshwater rivers and lakes in the Northern Hemisphere. However, the marine ancestor feeds predominantly on zooplankton, a resource typically sparse in rivers. The authors found that the head morphology of riverine stickleback differs remarkably from sticklebacks inhabiting lakes (i.e. a more marine-like environment with lots of zooplankton). When feeding on a natural zooplankton community, the authors determined via foraging tests and subsequent gut content analysis that lake stickleback outperform riverine stickleback in the capture of zooplankton. Furthermore, they linked capture success, particularly of evasive prey, to the degree of jaw protrusion. That means the longer the fish’s jaw protrudes towards the highly evasive zooplankton, the higher the chances of capture. What makes this study so remarkable is the rapidity of adaptive morphological differentiation since the two population sampled only diverged within the last 150 years.

In addition, the authors investigated the change in community composition as a consequence of predation by both lake and river-adapted stickleback and found that lake stickleback not only diminished the zooplankton community more readily than their riverine counterparts, but that they target largely predatory and highly evasive zooplankton, thus affecting the community structure and dynamics of their zooplankton prey. These results corroborate findings from a recent large-scale mesocosm experiment (Matthews et al. 2016 Current Biology). This means that traits such as jaw protrusion are a link between prey ecology and predator evolution and a mechanistic basis for feedbacks between the two.


Abstract

Identifying traits that underlie variation in individual performance of consumers (i.e. trait utility) can help reveal the ecological causes of population divergence, and the subsequent consequences for species interactions and community structure. Here, we document a case of rapid divergence (over the past 100 generations or ~150 years) in foraging traits and feeding efficiency between a lake and stream population pair of threespine stickleback. Building on predictions from functional trait models of fish feeding, we analyzed foraging experiments with a Bayesian path analysis and elucidated the traits explaining variation in foraging performance and the species composition of ingested prey. Despite extensive previous research on the divergence of foraging traits among populations and ecotypes of stickleback, our results provide novel experimental evidence of trait utility for jaw protrusion, gill raker length, and gill raker spacing when foraging on a natural zooplankton assemblage. Furthermore, we discuss how these traits might contribute to the differential effects of lake and stream stickleback on their prey communities, observed in both laboratory and mesocosm conditions. More generally, our results illustrate how the rapid divergence of functional foraging traits of consumers can impact the biomass, species composition, and trophic structure of prey communities.

Schnelle Ökotyp-Bildung eines Fischräubers verändert die Zusammensetzung der Zooplanktongemeinschaften

Um den Prozess der Artenbildung und dessen Wirkung auf die Struktur und Beziehungen ökologischer Gemeinschaften besser verstehen zu können, benötigt es detailierte Studien von Merkmalsvariationen und deren Funktionalität unter natürlichen Bedingungen. Wir dokumentieren hier den Fall einer besonders schnellen (~150 Jahre; <100 Generationen) Ökotyp-Formierung von Fluss- und See-angepassten Dreistachligen Stichlingen im Einzugsbereich des Bodensees (Schweiz). Die Ökotypen unterscheiden sich in Bezug auf ihre Kopfmorphologie und Effizienz der Nahrungsaufnahme maβgeblich: See-angepasste Stichlinge verschieben ihren Oberkiefer weiter nach vorne während der Öffnung des Mauls, fangen Zooplanktonbeute mit doppelter Effizienz und bevorzugen Ruderfusskrebse (Copepoda) an Stelle von Wasserflöhen (Cladocera). Interessanterweise lassen sich Variationen im Fraβerfolg auf unterschiedliche Kopfmorphologien zurückführen; genauer gesagt, dem Ausmaβ der Verschiebung des Oberkieferansatzes in Richtung der Beute und dem Abstand und der Länge der Bezahnung der Kiemenreusen. Zusätzlich, zeigt sich anhand von Labor- und Mesokosmos-Experimenten, dass Fluss- und See-angepasste Stichlinge die Gemeinschaft an Beutetieren unterschiedlich beeinflussen. Zuammenfassend gibt unsere Studie Aufschluss darüber, weshalb verschiedene Ökotypen der gleichen Art die trophische Struktur, Zusammensetzung und Häufigkeit ihrer Beute gegensätzlich beeinträchtigen können.