The potential for cleaner fish-driven evolution in the salmon louse Lepeophtheirus salmonis: Genetic or environmental control of pigmentation?

Abstract

The parasitic salmon louse represents one of the biggest challenges to environmentally sustainable salmonid aquaculture across the globe. This species also displays a high evolutionary potential, as demonstrated by its rapid development of resistance to delousing chemicals. In response, farms now use a range of non-chemical delousing methods, including cleaner fish that eat lice from salmon. Anecdotal reports suggest that in regions where cleaner fish are extensively used on farms, lice have begun to appear less pigmented and therefore putatively less visible to cleaner fish. However, it remains an open question whether these observations reflect a plastic (environmental) or adaptive (genetic) response. To investigate this, we developed a pigment scoring system and conducted complimentary experiments which collectively demonstrate that, a) louse pigmentation is strongly influenced by environmental conditions, most likely light, and b) the presence of modest but significant differences in pigmentation between two strains of lice reared under identical conditions. Based on these data, we conclude that pigmentation in the salmon louse is strongly influenced by environmental conditions, yet there are also indications of underlying genetic control. Therefore, lice could display both plastic and adaptive responses to extensive cleaner fish usage where visual appearance is likely to influence survival of lice.

Keywords: Lepeophtheirus salmonis; aquaculture; cleaner fish; environmental; genetic; pigmentation; plasticity.

FIGURE 1

Examples of pigment dispersion in L. salmonis pigment cells. Left: all pigments are in the core area of the pigment cell (unknown magnification), middle: pigments moderately dispersed, and right: pigments widely dispersed throughout the highly branched pigment cells. Middle and right photos: magn. 168×, scale bar 100 µm

FIGURE 2

Salmon louse pigmentation. From left to right: lice subjectively scored as less pigmented (type 1), medium pigmented (type 2), and heavily pigmented (type 3). The circle indicates the area on the louse where the louse MGV value was measured

FIGURE 3

Repeatability evaluation. Mean ± 95% confidence intervals of dMGV of 14 individual lice based on five repeated measurements

FIGURE 4

Influence of environmental light exposure (indoor/outdoor) on pigmentation in experiment 1. Data presented are the difference in mean gray value between a translucent background and the louse (dMGV), a measure of how much darker the louse is than the background. Faded points show dMGV measurements for each individual, while solid points and error bars display the fitted GLMM with 95% confidence intervals. Females are presented as shades of red and males as blue. Darker shades indicate the outdoor rearing environment, while light shades were reared indoors

FIGURE 5

Pigmentation in L. salmonis measured by two different methods: (a) Subjective pigment scores, showing the percent of dark lice (type 3) in the less pigmented strain and in the LsOslofjord strain, among males and females located dorsally and ventrally. Bars indicate 95% binominal confidence intervals (Zar, 1996). (b) dMGV: mean dMGV values for the area of a 50 pixel diameter circle on the cephalothorax. Bars represent 95% confidence intervals

FIGURE 6

Influence of parental population, individual louse size (cephalothorax length), position (dorsal/ ventral) and sex (M/F) on pigmentation in experiment 2. Dot points are the difference in mean gray value between a translucent background and the louse (dMGV) and measure how much darker the louse is than the background. Solid lines and shaded areas display the fitted GLMM with 95% confidence intervals. Females are presented as shades of red and males as blue. Darker shades indicate the “LsOslofjord” strain, while light shades indicate the “less pigmented” strain