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

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.

Keywords: Body size; ecological speciation; gape size; predator; trade‐off.

Figure 1

Map of Scandinavia showing the geographical distribution of the 358 lakes in our dataset.

Figure 2

Pike presence, lake area, and maximum depth control the formation of dwarf and giant whitefish ecotypes. (A) Maximum weight (kg) of whitefish from populations in lakes with (n = 217) and without (n = 103) pike as a function of lake area. Light blue symbols represent polymorphic whitefish populations for which each lake has two corresponding observations. (B) Classification tree (based on 13 explanatory variables, n = 350) for the prevalence of polymorphism in whitefish, showing that pike induces co‐occurring dwarf and giant ecotypes in lakes that are large and deep enough. The y‐axes show the number of lakes. Cohen's kappa for the whole model was 0.85.

Figure 3

Pike presence drives rapid body size divergence in whitefish. Coefficient of variation for lengths of mature whitefish in lakes with (n = 23) and without (n = 15) pike as a function of population age.

Figure 4

Rapid body size divergence leads the way to gill raker divergence. Between‐cluster differences (based on mature individuals caught in our standardized gillnet surveys, n = 19) in average values of body length and gill raker number as a function of population age. The positions of native populations were adjusted along the x‐axis to reduce overlap.

Figure 5

Body size divergence is associated with formation of benthic and pelagic ecotypes. Average length differences of sexually mature whitefish caught in littoral‐benthic and pelagic gillnets as a function of population age. Length differences were calculated as (mean littoral length‐mean pelagic length)/mean littoral length.

Figure 6

Whitefish spawning behavior is related to body size. Histogram showing the distribution of average body lengths for populations that spawn in stream habitat, shallow lake habitat (depth <4 m), or deep lake habitat (depth >4 m) (n = 72).

Figure 7

Large‐gaped predators can induce dwarf‐ and giant prey ecotypes by imposing a habitat choice‐growth strategy trade‐off. (A) Model simulation of maturation size as a function of predation intensity from a littoral predator capable of taking prey up to a maximum size of 18 cm. The red line represents giants that mature in the littoral habitat and the yellow line represents dwarfs that mature in the pelagic zone. (B) The range of predation intensities (which can be interpreted as predator density, see Table S6 for details) that induce evolutionary divergence at different values of maximum size of prey that can be taken by the predator. (C) The distribution of the giant ecotype between the pelagic habitat and the littoral habitat at the evolutionary stable state (ESS) when the littoral predator can take prey up to 18 cm and the predation intensity is 70%. The giants mature at 18.2 cm. (D) The corresponding distribution of the dwarf ecotype between the two habitats. Dwarfs mature at 9.7 cm.

Figure 8

Pike drives ecological speciation in whitefish. An illustration of the mechanisms whereby pike causes phenotypic divergence and ecological speciation in European whitefish.