Managing cryptic biodiversity: Fine‐scale intralacustrine speciation along a benthic gradient in Alpine whitefish (Coregonus spp.)

Abstract

Whitefish (Coregonus spp.) are an important catch for many freshwater fisheries, particularly in Switzerland. In support of this, supplemental stocking of whitefish species is carried out, despite lacking complete knowledge of the extent, distribution and origin of whitefish diversity in these lakes, potentially threatening local endemics via artificial gene flow. Here, we investigate phenotypic and genetic differentiation among coexisting whitefish species spawning along a depth gradient in a subalpine Swiss lake to better delineate intralacustrine whitefish biodiversity. We find depth‐related clines in adaptive morphology and in neutral genetic markers. This individual variation is structured in three distinct clusters with spatial overlap. Individual genetic distances correlate strongly with differences in growth rate and gill‐raker number, consistent with predictions of isolation‐by‐adaptation and ecological speciation. Genetic differentiation between species suggests reproductive isolation, despite demographic admixture on spawning grounds. Our results are consistent with clinal speciation resulting in three species coexisting in close ecological parapatry, one (C. sp. “benthic intermediate”) being previously unknown. A second unknown species spawning in close proximity was found to be of potential allochthonous origin. This study highlights the importance of taxonomically unbiased sampling strategies to both understand evolutionary mechanisms structuring biodiversity and to better inform conservation and fisheries management.

Rapid buildup of sympatric species diversity in Alpine whitefish

“…Within both lakes, none of the between‐species genetic structure was explained by geography, when considering the four species occurring in both lakes (Supporting Information Table ). This is consistent with earlier results from other Alpine whitefish radiations (Hudson et al., ; Vonlanthen et al., ). This may indicate that for highly mobile fish such as these, these postglacial lakes are too small for geographical genetic structure to arise.…”

“…Despite occurring in geographic sympatry, speciation in the latter case is still often associated with spatial ecological gradients at a smaller scale (Seehausen et al., ). Such fine‐scale structuring of ecological niches has been found to greatly facilitate speciation, both in empirical studies of adaptive radiations in fish (Hudson, Lundsgaard‐Hansen, Lucek, Vonlanthen, & Seehausen, ; Seehausen et al., ) and in theoretical models (Doebeli & Dieckmann, ; Gavrilets, ). It also plays a key role for the local coexistence of ecologically differentiated species in adaptive radiations that are assembled through allopatric speciation (Gillespie, ; Losos, ).…”

“…This large radiation is structured into multiple smaller monophyletic radiations, each located in a different lake system, hydrologically isolated from all others, and exhibiting similar sets of ecotypes (Hudson et al., ). Today, some Alpine lakes harbor up to five sympatric whitefish species (Hudson et al., ; Vonlanthen et al., ), and whitefish species richness of a lake is positively related to lake‐specific ecological and RI opportunity (Vonlanthen et al., ).…”

“…Low GRN are adaptive for feeding on benthic invertebrates and high GRN for feeding on zooplankton prey, as indicated by trait utility tests with sympatric Alpine whitefish species (Lundsgaard‐Hansen, Matthews, Vonlanthen, Taverna, & Seehausen, ; Roesch, Lundsgaard‐Hansen, Vonlanthen, Taverna, & Seehausen, ; B. Lundsgaard‐Hansen, C. Rösch, and O. Seehausen, unpublished data) and phenotype–environment correlations (Harrod et al., ; Kahilainen et al., ). Divergence along water depth occurs both outside the spawning season during feeding (Harrod et al., ; Steinmann, ), and very strongly during the spawning season on spawning grounds (Hudson et al., ; Vonlanthen et al., ). Furthermore, temporal (Steinmann, ) and spatial spawning segregation across lake habitats (Scandinavia, Østbye, Næsje, Bernatchez, Sandlund, & Hindar, ) can contribute to RI in whitefish.…”

Platichthys solemdali sp. nov. (Actinopterygii, Pleuronectiformes): A New Flounder Species From the Baltic Sea

“…in Europe and North America. In each lake where these taxa occur, species-pairs have evolved along depth gradients so that the two forms are distinguishable by molecular, morphological and physiological data (see Gagnaire et al, 2013;Hudson et al, 2017). In Europe some of these species-pairs show clear differences in reproductive ecology and are now considered as distinct species (Hudson et al, 2017).…”