Countergradient Variation and Secondary Sexual Color: Phenotypic Convergence Promotes Genetic Divergence in Carotenoid Use Between Sympatric Anadromous and Nonanadromous Morphs of Sockeye Salmon (Oncorhynchus Nerka)

Abstract

Abstract. Genetically distinct anadromous (sockeye) and nonanadromous (kokanee) morphs of the Pacific salmon, Oncorhynchus nerka, develop identical, brilliant red color at maturity during sympatric breeding in freshwater streams. The marine and lacustrine environments they occupy prior to maturity, however, appear to differ in the availability of dietary carotenoid pigments necessary to produce red coloration. We tested the hypothesis that kokanee, which occupy carotenoid-poor lakes, are more efficient at using the dietary pigments than are sockeye, which occupy the more productive North Pacific Ocean. In a 2-year controlled breeding study, flesh and skin color of mature and immature crosses fed a low-carotenoid diet were quantified with both a chromameter and by chemical extraction of carotenoid pigments. Results revealed striking countergradient variation in carotenoid use, with kokanee approximately three times more efficient at sequestering the pigments to the flesh musculature than similar age sockeye. This difference translated into virtually nonoverlapping differences between pure crosses in secondary sexual color at maturity, when the pigments are mobilized and transported to the skin. Kokanee crosses turned pinkish red over most of their body, whereas sockeye turned olive green. The olive green was similar to the breeding color of residuals in the wild, the progeny of anadromous sockeye that remain in fresh water and are believed to have given rise to kokanee on numerous independent occasions. Reciprocal hybrids were similar to each other and intermediate to the pure crosses, indicating additive genetic inheritance. Mate choice trials with sockeye males in the wild showed the ancestral morph strongly preferred red over green models. These results suggest a preference for red mates maintained in nonanadromous breeding populations drove the reevolution of the red phenotype in kokanee via more efficient use of dietary carotenoid pigments. This is a novel, yet hidden, mechanism by which sexual selection promotes the genetic differentiation of these sympatric populations.

Environmental Change, Phenotypic Plasticity, and Genetic Compensation

“…At sexual maturity, sockeye and kokanee both display intensely red carotenoid-based breeding coloration, but this similarity in coloration masks an important difference between the environments in which the two morphs develop. Carotenoid availability for salmon is probably much lower in the oligotrophic lakes inhabited by kokanee than in the ocean, where sockeye normally develop (Craig and Foote 2001). Residuals, the ancestral form of kokanee, are largely green at sexual maturity as a result of developing in the lowcarotenoid lacustrine environment.…”

Alternative reproductive strategies and the maintenance of female color polymorphism in damselflies

“…This idea has recently received considerable support, with increasing evidence suggesting that the pigments necessary to produce alternative colors may have pleiotropic effects on physiological attributes (Armbruster, 2002; Eliason, Shawkey, & Clarke, 2016; Forsman, Ringblom, Civantos, & Ahnesjö, 2002; Merrill, Van Schooten, Scott, & Jiggins, 2011; Roulin, Almasi, Meichtry‐Stier, & Jenni, 2011). Such alternative strategies have only been studied in a handful of male‐polymorphic organisms (Ahnesjo & Forsman, 2003; Hutchings & Myers, 1994; Lank, Smith, Hanotte, Burke, & Cooke, 1995; Tuttle, 2003) and in three female‐polymorphic organisms: butterflies (Ellers & Boggs, 2002), fishes (Craig & Foote, 2001), and recently, reptiles (Galeotti et al., 2013). In ischnuran damselflies, evidences for the link between color and behavior come from two studies with Ischnura ramburii (Sirot, Brockmann, Marnis, & Muschett, 2003) and I. elegans (Van Gossum, Stoks, & De Bruyn, 2001a).…”

Countergradient Variation in the Sexual Coloration of Guppies (Poecilia Reticulata): Drosopterin Synthesis Balances Carotenoid Availability

“…A female preference for hue has not yet been demonstrated, but guppies of both sexes are innately attracted to orange objects in preference to other colors (including yellow and red), and this sensory bias appears to be linked to the mate preference for orange coloration (Rodd et al 2002). If drosopterin production has evolved along the carotenoid availability gradient in response to a hue-based female preference, this would be an example of countergradient variation caused by sexual selection (see also Craig and Foote 2001).…”