Selection from visual predation vs. developmental plasticity of isopod pigmentation

Divergent selection and adaptive phenotypic plasticity can jointly influence phenotypic differentiation within and among populations. Understanding how these processes interact is difficult when the same environmental differences that lead to divergent selection can also promote phenotypic plasticity. Previous work has shown that pigmentation of the freshwater isopod Asellus aquaticus varies with background colour (Hargeby et al. 2004). This is hypothesized to be an evolutionary response to visual predation along a gradient of differently coloured macrophyte-backgrounds.

In an six month long outdoor mesocosm experiment, we investigated how predator density (0, 30, and 60 threespine stickleback per mesocosm) and macrophytes (presence/absence) affected the abundance and pigmentation of isopods. While we found that fish presence strongly reduced isopod density, particularly in the absence of macrophytes, we found no effect on the size or pigmentation of isopods (Lürig et al. 2019). Instead, we detected increased pigmentation in the presence of macrophytes, and across all levels of fish density. A subsequent laboratory rearing experiment indicated that pigmentation of isopods may a developmentally plastic trait (Lürig et al. 2019).

Figure 1 - Left: Macrophyte presence yielded higher pigmentation (size corrected) in isopods than macrophyte-free tanks, independent of fish presence. Each data point represents the average response for one mesocosm and the large dots with error bars are mean ± CI per treatment across all mesocosms with. The solid line indicates the mean starting condition, and the dashed lines show mean and SD of the starting populations, respectively. Mid: rates of increase in pigmentation were higher under high-nutrient diet (dots = weekly average change in pigmentation or body size of individuals across all families [mean ± CI], grey lines = family- level reaction norms). Right: In summary, results from both of our experiments suggests that pigmentaion can be affected by the presence of macrophytes, and by elevated protein content within the diet.

Inspired by the findings of our mesocom experiment, we investigated whether developmental phenotypic plasticity could be responsible divergent patterns of pigmentation. In a laboratory experiment we reared over 1000 individuals from 29 families with two diets of contrasting nutritional quality (low/high protein concentration), and quantified developmental trajectories of body size and pigmentation for every individual for 12 weeks. Overall, dietary protein had strong effects on the developing phenotype, and this influenced the “survival landscape” of juvenile isopods. Specifically, we found that higher dietary protein had strong positive effects on the developmental rate of pigmentation, but led to increased mortality under high growth and pigmentation rates. Building on previous work, suggesting that visual predation has mediated the evolution of A. aquaticus body size and cryptic pigmentation, our study shows how dietary effects on the developmental trajectories of juvenile isopods can have fitness consequences in the absence of predation.

Currently in review

Figure 2 - A) Random sample of isopods taken from beds of Chara tomentosa in Lake Lucerne at Kastanienbaum (measured with a flatbed scanner, brightness adjusted to match images from camera stand; size scale is for panel A-C.). B) Example of an isopod reared under low quality and C) high quality diet (photographed with a camera-stand). The levels of adult isopod pigmentation measured throughout the diet manipulation fall well within the range of isopod pigmentation found in nature (i.e. panel A).

Literature

Hargeby, A., J. Johansson, and J. Ahnesjö. 2004. Habitat-specific pigmentation in a freshwater isopod: adaptive evolution over a small spatiotemporal scale. Evolution; international journal of organic evolution 58:81–94.

Lürig, M. D., R. J. Best, M. Svitok, J. Jokela, and B. Matthews. 2019. The role of plasticity in the evolution of cryptic pigmentation in a freshwater isopod. The Journal of animal ecology 88:612–623.