Lack of specialization in trophic morphology between genetically differentiated dwarf and normal forms of lake whitefish (Coregonus clupeaformis Mitchill) in Lac de IyEsty Quebec

We recently observed a bimodal distribution in size of sexually maturing lake whitefish (Coregonus clupeaformis Mitchill) in Lac de L'Est, Quebec. The objective of this study was to test the hypothesis that these two spawning size classes represent genetically distinct ecotypes, potentially adapted in morphology for occupying different trophic niches. This was accomplished by quantifying the extent of genetic (mitochondrial DNA (mtDNA) and enzyme loci) and morphological differences. Significant differences in haplotype and allele frequency distributions confirmed the hypothesis that whitefi'sh maturing at small (dwarf) and normal sizes are structured into two distinct gene pools. However, low F,, values at mtDNA and enzyme loci, coupled with the apparent lack of spatial and temporal spawning segregation, suggest that reproductive isolation is incomplete and that gene flow is still occurring between the two forms. Patterns of mtDNA diversity favoured the origin of genetically distinct dwarf and normal-size lake whitefish forms in Lac de 1'Est through sympatric divergence. However, a lack of differences in morphological traits potentially related to trophic ecology did not support the hypothesis that the two forms represent ecotypes which are morphologically specialized in trophic niches. This study established that sympatric dwarf and normal-size spawning groups of lake whitefish in Lac de 1'Est represent two genetically distinct populations despite the potential for gene flow between them. This, coupled with their low level of morphological diversification, suggests that they represent an early stage of population divergence, and therefore makes them of particular interest for understanding the gene environment processes involved in the early steps of speciation events. RCsumC : Nous avons rCcemment observC une bimodalit6 dans la distribution de la taille des Grands corkgones (Coregonus clupeaformis Mitchill) en cours de maturation sexuelle dans le Lac de I'Est, QuCbec. L'objectif de cette Ctude Ctait de vCrifier l'hypothkse voulant que ces deux classes de taille reprksentent des Ccotypes gCnCtiquement diffCrenciCs qui posskdent une morphologie potentiellement adaptCe a I'utilisation diffkrentielle de niches trophiques. Pour ce faire, nous avons quantifiC leur degrC de diffkrenciation gCnCtique (ADN mitochondrial et loci enzymatiques) et morphologique. Des diffkrences significatives ont CtC observkes dans la distribution des frkquences allCliques aux deux types de marqueurs, confirmant ainsi que l'hypothkse que les corCgones qui atteignent leur maturitC a une petite et grande tailles sont structurCs en deux pools gCnCtiques distincts. Cependant, les faibles valeurs de Fs, observCes, jumelees a I'absence apparente de sCgrCgation spatiale et temporelle au moment de la reproduction, suggkrent que I'isolement reproducteur est incomplet et qu'un flux gCnique se maintient entre les deux formes. Le comportement de la diversit6 mitochondriale favorise I'hypothkse d'une origine sympatrique de ces deux formes. Cependant, l'absence de diffkrences au niveau des traits morphologiques potentiellement reliCs a 1'Ccologie trophique ne supporte pas 17hypothkse que ces deux formes reprksentent des Ccotypes morphologiquement spCcialisCs pour 170ccupation de niches distinctes. En conclusion, 17ensemble de ces rCsultats suggkre que les formes sympatriques du coregone du Lac de 1'Est representent un stade primaire de divergence des populations, ce qui en fait un systkme d7intCrCt particulier pour la comprChension des interactions gCnome-environnement impliquees dans les premiers stades du phenomkne de la spCciation. Introduction Indeed, they provide an opportunity to observe the effects of evolutionary forces promoting reproductive isolation (Mallet of exchanging genes but showing 1995). However, such situations are relatively rare, and conthe to retain gene pools are of particular sequently, speciation studies have more often relied on the interest for the stages of formation. comparison of closely related yet fully isolated species (Otte Received November 10, 1995. Accepted May 5, 1996. and ~ n d l e r 1989). A major drawback of such an approach is that it is more likely to provide information about the charac. A* Chouinard, Pigeon, and Lo Bernatchez.' DCpartement teristics of species than about the processes that gave rise to de biologie, Groupe interuniversitaire de recherches them (McPhail 1993). Therefore, it is still relevant to idenocCanographiques du QuCbec (GIROQ) , UniversitC Lava1 , tify populations between which reproductive barriers may Sainte-Foy , PQ G1K 7P4, Canada. have begun to develop but are still incomplete. ' Author to whom all correspondence should be addressed In fishes, the sympatric occurrence of closely related (e-mail: [email protected]). forms belonging to the same species complex probably proCan. J . Zool. 74: 19891998 (1996). Printed in Canada / ImprimC au Canada Can. J. Zool. Vol. 74, 1996 Fig. 1. Location of Lac de 1'Est. vides the best available models to study genetic, ecological, and behavioural changes that may occur during species formation (Skulason and Smith 1995). This phenomenon has been reported in several temperate-zone and northern freshwater species but remains unusual (e.g., Bodaly 1979; Ferguson and Mason 198 1 ; Lindsey and Klatt 1982; Galat and Vucinich 1983; Verspoor and Cole 1989; Taylor and Bentzen 1993a, 1993b; Schluter and McPhail 1993; Snorrason et al. 1994). The lake whitefish (Coregonus clupeaforrnis Mitchill) constitutes one of the species complex in which the occurrence of sympatric forms has been observed at several locations in North America, including southern Yukon (Lindsey 1963; Lindsey et al. 1970; Bodaly et al. 1988), northern Maine (Fenderson 1964), Ontario (Kennedy 1943; Bodaly et al. 1991a), Quebec (Fortin and Gendron 1990), and Labrador (Bodaly et al. 1992). As in most other groups of fish in which sympatric forms have been investigated, studies in lake whitefish have indicated that ecological, behavioural, and morphological differences between sympatric forms are functionally related and are apparently adaptations for occupying different trophic niches (e. g . , Bodaly 1979); this suggests that opportunities for using distinct food resources may be an important mechanism driving ecotypic radiation in fish (Schluter and McPhail 1993). Genetic analyses of isozyme and mitochondrial DNA (mtDNA) variation have also indicated that sympatric whitefish ecotypes are genetically differentiated to variable degrees, and may constitute reproductive units having the capacity to retain separate gene pools despite the potential for hybridization (Kirkpatrick and Selander 1979; Bernatchez and Dodson 1990; Vuorinen et al. 1993; Bernatchez et al. 1996). Therefore, detailed ecological, morphological, and genetic studies of these populations During a search for a more accessible system where such studies could be undertaken, we observed a strong bimodal distribution in sizes of sexually maturing lake whitefish in Lac de 1'Est (Quebec), which suggested the existence of sympatric forms in this lake. The objective of this study was to test the hypothesis that these two spawning size classes of lake whitefish represent genetically distinct ecotypes that are potentially adapted in morphology for occupying different trophic niches. This was accomplished by quantifying the extent of genetic (mtDNA and isozymps) and morphological differences between fish belonging to the two spawning groups. Material and methods Study area and sampling Lac de 1'Est is part of the St. John River drainage and is located 120 km east of Quebec City (47" 15'N, 69"301W), near the town of Mont-Carmel (Fig. 1). The lake is 9.1 km long with a surface area of 726 ha, and has a mean and a maximum depth of 14.7 and 36.7 m, respectively. The fish community is dominated by lake whitefish, and the two main predators are burbot (Lota lota) and lake trout (Salvelinus namaycush). Lake cisco (Coregonus artedi) is absent from the lake. Lake whitefish were captured at the bottom, surface, and midwater from 15 to 19 June 1993, using 63 x 1.8 m gill nets comprising nine panels graded from 1.25 to 7.6 cm mesh size (stretched measure) set out overnight. Fish were measured and weighed, and stage of gonad development was estimated according to Nikolskii (1963). Lake whitefish that had reached stage 3 of gonad development were considered potential spawners for the fall of the same year (Morin et al. 1982). Maturing fish of the two spawning size groups were kept at -80°C prior to genetic and morphological analyses. For convenience, in the text we designate the two spawning size groups as dwarf and normal forms. could increase our knowledge of gene -environment inter~ i ~ ~ ~ h ~ ~ d ~ i ~ l DNA analysis during the Total DNA was extracted from either the eggs or the liver of 41 these have been undertaken thus far, because normal and 38 dwarf lake whitefish as described previously by of the difficulty of accessing (because of either ~emoteness Bernatchez et al. (1992). Two segments of the mitochondrial or legislation) those lakes harbouring whitefish sympatric genome encompassing the ND-516 region (2.4 kilobase pairs) and forms reported to date. the cytochrome blcontrol region (D-loop) (2.1 kilobase pairs) were