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

Abstract

<jats:title>Abstract</jats:title><jats:p>Lake-dwelling fish that form species pairs/flocks characterized by body size divergence are important model systems for speciation research. While 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 reconstructed the initial stages of speciation in European whitefish (<jats:italic>Coregonus lavaretus</jats:italic>) using data from 357 populations of varying age (26-10 000 years). We find that whitefish speciation is driven by a large-growing predator, the northern pike (<jats:italic>Esox lucius</jats:italic>). 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.</jats:p>

Competition among small individuals hinders adaptive radiation despite ecological opportunity

“…Disruptive selection and subsequent speciation can arise from frequency-dependent interactions other than intraspecific resource competition. Other factors promoting divergence in populations include predation [12,53,54] and mutualistic interactions [10]. Since predation is often habitat- and size-specific (e.g.…”

Multidimensional divergent selection, local adaptation, and speciation

“…Although there are good examples of quantification for the present, the past is rarely considered (Öhlund et al. 2020). This is problematic because theory shows that where multiple species coexist at evolutionary equilibrium, a single key change (unidimensional divergence) can destabilize evolutionary equilibria and so cause co‐evolutionary ripple effects that lead to multidimensional divergence in response to biotic selection pressures, conflating cause and effect (Gilman et al.…”

“…A study of present‐day conditions could thus implicate multidimensional selection, whereas this was not the primary cause of divergence (Öhlund et al. 2020). Furthermore, it is important to consider that present‐day divergence on one environmental/trait axis might be the end point of many possible adaptive trajectories with implications for genomic parallelism and transgressive incompatibilities (Chevin et al.…”

Genetic relationships between sympatric and allopatric Coregonus ciscoes in North and Central Europe

“…The Holarctic genus Coregonus (whitefishes and ciscoes) is particularly diverse [15], with numerous examples of sympatric pairs or species flocks that have evolved after the last glaciations [16][17][18]. Coregonus are considered typical examples for incipient and ongoing speciation events in post-glacial lakes, induced by segregation along ecological gradients, such as lake habitats (littoral, pelagic and profundal habitats) and feeding niches (planktivory, benthivory, and occasionally piscivory), by physiological differences along vertical temperature gradients, or by predator-induced morphological divergence [16,19,20]. It is generally assumed that similar trajectories of ecological divergence found in different lakes would support independent sympatric speciation from a single ancestor [21].…”

“…Only bootstrap values > 50% are shown. Three main clusters of populations, as discussed in the text, are displayed (Cluster I and II are corresponding to the population assemblages I and II identified by Delling et al[20]). The colored dots refer to the sampling locations in Fig.1…”