Evolution without standing genetic variation: change in transgenerational plastic response under persistent predation pressure

Abstract

Transgenerational phenotypic plasticity is a fast non-genetic response to environmental modifications that can buffer the effects of environmental stresses on populations. However, little is known about the evolution of plasticity in the absence of standing genetic variation although several non-genetic inheritance mechanisms have now been identified. Here we monitored the pea aphid transgenerational phenotypic response to ladybird predators (production of winged offspring) during 27 generations of experimental evolution in the absence of initial genetic variation (clonal multiplication starting from a single individual). We found that the frequency of winged aphids first increased rapidly in response to predators and then remained stable over 25 generations, implying a stable phenotypic reconstruction at each generation. We also found that the high frequency of winged aphids persisted for one generation after removing predators. Winged aphid frequency then entered a refractory phase during which it dropped below the level of control lines for at least two generations before returning to it. Interestingly, the persistence of the winged phenotype decreased and the refractory phase lasted longer with the increasing number of generations of exposure to predators. Finally, we found that aphids continuously exposed to predators for 22 generations evolved a significantly weaker plastic response than aphids never exposed to predators, which, in turn, increased their fitness in presence of predators. Our findings therefore showcased an example of experimental evolution of plasticity in the absence of initial genetic variation and highlight the importance of integrating several components of non-genetic inheritance to detect evolutionary responses to environmental changes.

Fig. 1

Proportions of winged adult aphids (mean ± SE) across generations of the experimental evolution with predators (in red), without predators (in black) and in branch lines for which predators were removed after generations 3, 13, and 22 (in blue). “*” or “NS” denote the significance (P < 0.05, or P > 0.05, respectively) of differences between controls (without predator, black dots) and branch lines after predator removal (blue dots). The vertical black dotted line indicates the time of initial predator introduction in the treatment lines

Fig. 2

Relationship between the number of generations exposed to predators and the number of generations needed for the proportion of winged aphids to come back to the control level after predator removal (see Text S2 for more details about the method used to estimate y-axis values for each predator removal)

Fig. 3

Aphid population growth rate (mean ± SE) across generations in the experimental evolution with predators (in red), without predators (in black) and in the branch lines for which predators were removed after generations 3, 13, and 22 (blue lines). “*” and “NS” denote significance (P < 0.05, or P > 0.05, respectively) of differences between the control without predator (black dots) and the treatment in which predators were removed (blue dots) at a given generation. The vertical black dashed line indicates the time of initial predator introduction in treatment lines

Fig. 4

Relationship between the proportion of winged adult aphids and the population growth rate in the main experimental lines (a) without (black dots and full black line) and with predators (red dots and dashed red line), and (b) in the branch experimental lines for which predators were removed after generations 3 (light blue dots and full light blue line), 13 (blue dots and short-dashed blue line), and 22 (dark blue dots and long-dashed dark blue line). Repeated measures correlation tests (Bakdash and Marusich 2017): main experimental lines without predators (r = −0.11 df = 233, p = 0.09); main experimental lines with predators (r = −0.23, df = 233, p = 0.0004); branch experimental lines for which predators were removed after generations 3 (r = −0.38, df = 35, p = 0.02), 13 (r = −0.79, df = 35, p < 0.0001), and 22 (r = −0.73, df = 35, p < 0.0001)

Fig. 5

Change in aphid plastic response and population growth rate between the 16th and the 25th generation of experimental evolution. Here we illustrate the differences in plasticity in the additional experiments for experimental lines that were isolated after 16 and 25 generations of experimental evolution (first and second column, respectively). Changes in proportions of winged adult aphids (mean ± SE) are represented in a and b, and changes in aphid population growth rates (mean ± SE) are represented in c and d. The plastic response is observed across environments (absence and presence of predators corresponding to the Test Predation Treatment represented on the x-axes) by comparing the change in the phenotype values represented along the y-axes for aphids continuously exposed or never exposed to predators (red and black dots, respectively) during experimental evolution. “*” or “NS” denote significance (P < 0.05, or P > 0.05, respectively) of differences between evolutionary predation treatments (i.e., the presence/absence of predators during experimental evolution)