Functional and evolutionary trade-offs co-occur between two consolidated memory phases in Drosophila melanogaster

Abstract

Memory is a complex and dynamic process that is composed of different phases. Its evolution under natural selection probably depends on a balance between fitness benefits and costs. In Drosophila, two separate forms of consolidated memory phases can be generated experimentally: anaesthesia-resistant memory (ARM) and long-term memory (LTM). In recent years, several studies have focused on the differences between these long-lasting memory types and have found that, at the functional level, ARM and LTM are antagonistic. How this functional relationship will affect their evolutionary dynamics remains unknown. We selected for flies with either improved ARM or improved LTM over several generations, and found that flies selected specifically for improvement of one consolidated memory phase show reduced performance in the other memory phase. We also found that improved LTM was linked to decreased longevity in male flies but not in females. Conversely, males with improved ARM had increased longevity. We found no correlation between either improved ARM or LTM and other phenotypic traits. This is, to our knowledge, the first evidence of a symmetrical evolutionary trade-off between two memory phases for the same learning task. Such trade-offs may have an important impact on the evolution of cognitive capacities. On a neural level, these results support the hypothesis that mechanisms underlying these forms of consolidated memory are, to some degree, antagonistic.

Figure 1.

Experimental selection design. From a natural population, 16 lines were conditioned in the Pavlovian olfactory paradigm for each memory type (eight ARM with eight control lines and eight LTM with eight control lines); then 24 h later, memory retention was tested in a T-maze. Only flies that made the correct choice were kept to breed the next generation. A random selection of control flies, corresponding to the number of selected flies that made the correct choice were kept to breed.

Figure 2.

Evolution of the difference in memory scores (mean ± s.e.m. based on variation among lines) between selected and control lines over the course of the selection regime. Memory scores have been grouped into sets of four generations for graphical purposes. Black circles, selection regime LTM; grey circles, selection regime ARM.

Figure 3.

(i) Generation 23 and (ii) generation 28. Memory scores 24 h after massed or spaced conditioning for control (open bars) and selected (filled bars) (a) ARM or (b) LTM lines using mechanical shock as the US (mean ± s.e.m. based on variation among lines, n = 5–9 per replicate line). *p < 0.05; **p < 0.01; ***p < 0.001.

Figure 4.

Generation 30. Memory scores 24 h after massed or spaced conditioning for (a) control (open bars) and selected ARM (filled bars) or (b) control (open bars) and selected LTM (filled bars) lines using electric shock as the unconditioned stimulus (mean ± s.e.m. based on variation among lines, n = 5–9 per replicate line). *p < 0.05; **p < 0.01; ***p < 0.001.

Figure 5.

Generation 30. Correlated response in longevity to selection for improved LTM. (a) Age-specific survival for virgin females (left panel) and males (right panel) of control and selected lines is expressed by the mean proportion of flies alive ± s.e.m. (open diamonds, control; filled diamonds, selected). (b) Age-specific mortality rate for both selected and control lines for males and females (open circles, control; filled circles, selected). Regression lines represent the most parsimonious logistic model for each sex.

Figure 6.

Generation 30. Correlated response in longevity to selection for improved ARM. (a) Age-specific survival for virgin females (left panel) and males (right panel) of control and selected lines is expressed as the mean proportion of living flies ± s.e.m. (open diamonds, control; filled diamonds, selected). (b) Age-specific mortality rate for both selected and control lines for males and females (open circles, control; filled circles, selected). Regression lines represent the most parsimonious logistic model for each sex.