Ecological speciation in European whitefish is driven by a large-gaped predator.

Gunnar Öhlund,Göran Englund,Åke Brännström,Mikael Peedu,Karin A Nilsson,Alan G Hudson,Catherine L Hein,Mats Bodin,Pia Bartels,Kim Præbel,Sven-Ola Öhlund,Petter Johansson,Kenyon B Mobley

doi:10.1002/evl3.167

Abstract

Lake‐dwelling fish that form species pairs/flocks characterized by body size divergence are important model systems for speciation research. Although several sources of divergent selection have been identified in these systems, their importance for driving the speciation process remains elusive. A major problem is that in retrospect, we cannot distinguish selection pressures that initiated divergence from those acting later in the process. To address this issue, we studied the initial stages of speciation in European whitefish (Coregonus lavaretus) using data from 358 populations of varying age (26–10,000 years). We find that whitefish speciation is driven by a large‐growing predator, the northern pike (Esox lucius). Pike initiates divergence by causing a largely plastic differentiation into benthic giants and pelagic dwarfs: ecotypes that will subsequently develop partial reproductive isolation and heritable differences in gill raker number. Using an eco‐evolutionary model, we demonstrate how pike's habitat specificity and large gape size are critical for imposing a between‐habitat trade‐off, causing prey to mature in a safer place or at a safer size. Thereby, we propose a novel mechanism for how predators may cause dwarf/giant speciation in lake‐dwelling fish species.

Highlights

Understanding the mechanisms causing ecological speciationwith-gene-flow is challenging because the phenomenon cannot be directly observed in natural systems
Examples of ongoing ecological speciation in sympatry are especially common in lake-dwelling fish, as they have an intriguing propensity to form genetically distinct ecotypes that differ in ecology, morphology, and reproductive biology (Skulason and Smith 1995; Seehausen and Wagner 2014)
We present extensive comparative data showing that northern pike is the key driver of ecological speciation in Scandinavian whitefish populations, and use data from populations of different age and modelling to form a hypothesis for why this large-growing predator is so critically important

Summary

Introduction

Understanding the mechanisms causing ecological speciationwith-gene-flow is challenging because the phenomenon cannot be directly observed in natural systems. Data from 358 populations of European whitefish, and find that ecological speciation in this well-studied model system is driven by a previously unrecognized selective agent, the northern pike To understand how this large-growing predator initiates divergence, we analyze a chronosequence of replicated speciation events (26–10,000 years old). There is substantial variation among ecosystems and species as to how far this divergence has progressed (Hendry et al 2009; Nosil et al 2009), but a common feature is the evolution of large- and small growing ecotypes along resource and/or habitat gradients in the lake environment. If some ecological mechanism drives individuals to specialize in different habitats, this can cause divergent selection and conspicuous adaptations that are by-products rather than drivers of the initial divergence

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