Transgenerational plasticity of dispersal‐related traits in a ciliate: genotype‐dependency and fitness consequences

Abstract

Phenotypic plasticity, the ability of one genotype to produce different phenotypes in different environments, plays a central role in species' response to environmental changes. Transgenerational plasticity (TGP) allows the transmission of this environmentally-induced phenotypic variation across generations, and can influence adaptation. To date, the genetic control of TGP, its long-term stability, and its potential costs remain largely unknown, mostly because empirical demonstrations of TGP across many generations in several genetic backgrounds are scarce. Here, we examined how genotype determines the TGP of phenotypic traits related to dispersal, a fundamental process in ecology and evolution. We used an experimental approach in Tetrahymena thermophila, a ciliate model-species, to determine if and how phenotypic changes expressed following a dispersal treatment are inherited over multiple generations. Our results show that morphological and movement traits associated with dispersal are plastic, and that these modifications are inherited over at least 35 generations. The fitness costs and benefits associated with these plastic changes are also transmitted to further generations. We highlight that the genotype modulates the expression and reversibility of transgenerational plasticity of dispersal-related traits and its fitness outcomes. Our study thus suggests that genotype-dependent TGP could play an important role in eco-evolutionary dynamics as dispersal determines gene flow and the long-term persistence of natural populations.

Temperature‐mediated transgenerational plasticity influences movement behaviour in the green algae Chlamydomonas reinhardtii

“…However, the extent to which TGP can modify behaviours of multiple generations remains comparatively underexplored. Our results do add to a small list of studies that have documented TGP influencing behaviours across multiple generations; for example, dispersal-related effects on swimming speed and cell morphology of Tetrahymena thermophila persisted for up to 35 generations (Cayuela et al, 2022). As such, the persistent effects we observed among cold (12.5°C)-and hot (37.5°C)-acclimated populations assayed in warm (25°C) environments are among the most sustained durations of behavioural TGP recorded to date.…”

“…However, the extent to which TGP is capable of influencing behaviour—that is, the coordinated responses of whole living organisms or groups of organisms to internal or external stimuli, excluding developmental responses (Levitis et al, 2009)—remains comparatively understudied (e.g. Allan et al, 2013; Cayuela et al, 2022; Crill et al, 1996; Le Roy et al, 2017; Le Roy & Seebacher, 2018; Seebacher et al, 2014; Snell‐Rood, 2013).…”

Phenotypic plasticity and the effects of thermal fluctuations on specialists and generalists

“…thermophila is a 20 to 50 µm ciliate naturally living in freshwater ponds and streams [35,36]. Previous studies provided evidence for differences between genotypes in thermal tolerance curves [30,31] and phenotypic plasticity of morphological and movement traits [30,31,[37][38][39]. Moreover, thermal fluctuations are known in this species to affect population dynamics and the evolution of heat shock protein Hsp90 expression [40].…”

“…Here, we used 15 strains originally sampled in the early 2000s from different locations in North America [41]. Isogenic strains reproduce clonally in laboratory conditions, meaning that for a given clonal strain, differences in trait values after 2 h between replicated environmental conditions result from the expression of phenotypic plasticity [31,39,42]. Cells were maintained in axenic liquid growth media (0.6% Difco Proteose Peptone, 0.06% yeast extract) at 23°C, a classic laboratory maintenance condition for this species [43,44].…”

Dispersal plasticity driven by variation in fitness across species and environmental gradients

“…Dispersal reaction norms were established from the quantification of dispersal rates in standard two‐patch microcosms (Figure S1 ) consisting of Eppendorf microtubes (1.5 ml) linearly connected by a corridor (4 mm internal diameter silicon tube, 2.5 cm long) filled with 2.8 ml of growth media. These two‐patch systems, in which environmental conditions are kept spatially homogeneous, are classically used to quantify emigration decisions (Cayuela et al, 2022 ; Fjerdingstad et al, 2007 ; Jacob, Chaine, et al, 2015 ; Junker et al, 2021 ; Pennekamp et al, 2014 ). One of the two patches was inoculated at 10% of a genotype's maximal density (150 μl of 1‐week old culture).…”