Facultative parasites as evolutionary stepping-stones towards parasitic lifestyles

Abstract

Parasites and parasitic lifestyles have evolved from free-living organisms multiple times. How such a key evolutionary transition occurred remains puzzling. Facultative parasites represent potential transitional states between free-living and fully parasitic lifestyles because they can be either free-living or parasitic depending on environmental conditions. We suggest that facultative parasites with phenotypically plastic life-history strategies may serve as evolutionary stepping-stones towards obligate parasitism. Pre-adaptations provide a starting point for the transition towards opportunistic or facultative parasitism, but what evolutionary mechanism underlies the transition from facultative to obligate parasitism? In this Opinion Piece, we outline how facultative parasites could evolve towards obligate parasites via genetic assimilation, either alone or in combination with the Baldwin effect. We further describe the key predictions stemming from each of these evolutionary pathways. The importance of genetic assimilation in evolution has been hotly debated. Studies on facultative parasites may not only provide key insights regarding the evolution of parasitism, but also provide ideal systems in which to test evolutionary theory on genetic accommodation.

Keywords: Baldwin effect; evolution of parasitism; genetic accommodation; genetic assimilation; opportunistic pathogens; phenotypic plasticity.

Figure 1.

Illustration of three scenarios of genetic accommodation in facultative parasites. (a(i), b(i) and c(i)) Ancestral, free-living populations that exhibit an increased probability of exhibiting a parasitic lifestyle when exposed to novel environmental conditions. (a(ii), b(ii) and c(ii)) Current populations following genetic accommodation. (a) The Baldwin effect. Expected phenotypes for the population if phenotypic plasticity exhibited in the ancestral population was adaptive, but was less than the optimal level of parasitism. Plasticity provided the opportunity for natural selection to act on heritable variants such that the mean phenotypic value further increased in the novel environment. Whether selection for higher trait expression in the novel environment is associated with concurrent changes in the mean trait expression in the ancestral environment will depend on the extent of genetic correlation between intercept and slope (illustrated by the grey region). Note that the Baldwin effect alone (shown in c(ii)) would not lead to complete loss of the free-living lifestyle. (b) Genetic assimilation. Plasticity exhibited by the ancestral population produced the optimal phenotype in the novel environment, in this case, 100% chance of adopting a parasitic lifestyle. Selection then acted to reduce phenotypic plasticity, such that the novel trait (parasitism) no longer requires the novel environmental cue to induce its expression. The current population is exclusively parasitic across all environments (i.e. obligate parasites). (c) Genetic assimilation and the Baldwin effect. The evolution of obligate parasitism occurred via selection on mean propensity to behave parasitically in the novel environment, coincident with selection for reduced plasticity.

Figure 2.

Illustration of how facultative parasites could be used to address questions related to the costs of plasticity by studying clades that contain free-living species (FL), facultative parasites (FP) and obligate parasites (OP). FL exhibit the free-living phenotype and OP exhibit the parasitic phenotype regardless of environmental conditions. However, FP can be induced to exhibit either a free-living phenotype (typically under benign environmental conditions) or a parasitic phenotype (typically under stressful conditions). (a) No costs to plasticity: the FP exhibiting a free-living phenotype achieve equal fitness to FL under benign environmental conditions, and FP exhibiting the parasitic phenotype achieve the same fitness as OP under stressful environmental conditions. (b) Costs to plasticity: FP always achieve lower fitness than the non-plastic species exhibiting the same phenotype.