Can ecological changes impact somatic genome development? Efforts to resolve this question could reveal a direct link between environmental changes and somatic variability, potentially illuminating our understanding of how variation can surface from a single genotype under stress. Here, we tackle this question by leveraging the biological properties of ciliates. When Paramecium tetraurelia reproduces sexually, its polyploid somatic genome regenerates from the germline genome through a developmental process that involves the removal of thousands of ORF-interrupting sequences known as internal eliminated sequences (IESs). We show that exposure to nonstandard culture temperatures impacts the efficiency of this process of programmed DNA elimination, prompting the emergence of hundreds of incompletely excised IESs in the newly developed somatic genome. These alternative DNA isoforms display a patterned genomic topography, impact gene expression, and might be inherited transgenerationally. On this basis, we conclude that environmentally induced developmental thermoplasticity contributes to genotypic diversification in Paramecium.

Unicellular organisms such as ciliates are largely neglected in research on adaptive developmental plasticity, although their nuclear dualism offers ideal circumstances to study development outside an embryonic context. Here, we gain first insights into the ability of the ciliate Paramecium to develop potentially adaptive phenotypic changes in response to early-life adversity. We show that, upon exposure to unconventional culture temperatures, germ line-to-soma differentiation gives rise to coordinated molecular changes that may help attune the number of functional gene copies to the new external conditions. The non-random somatic heterogeneity that developmental plasticity generates is largely epigenetically controlled, shaped by the parental experience, and may prompt a stress response. These findings establish Paramecium as a new model system to study the molecular basis and evolutionary significance of developmental plasticity. In echoing previous indications in mammals, they call for an incorporation of intergenerational effects in adaptation studies.

19The impact of ecological changes on the development of new somatic genomes has 20 thus far been neglected. This oversight yields an incomplete understanding of the 21 mechanisms that underlie environmental adaptation and can be tackled leveraging the 22 biological properties of ciliates. When Paramecium reproduces sexually, its polyploid 23 somatic genome regenerates from the germline genome via a developmental process, 24 Programmed DNA elimination (PDE), that involves the removal of thousands of ORF-25 interrupting germline sequences. Here, we demonstrate that exposure to sub-optimal 26 temperatures impacts PDE efficiency, prompting the emergence of hundreds of 27 alternative DNA splicing variants that dually embody cryptic (germline) variation and 28 de novo induced (somatic) mutations. In contrast to trivial biological errors, many of 29 these alternative DNA isoforms display a patterned genomic topography, are 30 epigenetically controlled, inherited trans-somatically, and under purifying selection. 31Developmental thermoplasticity in Paramecium is a likely source of evolutionary 32 innovation. 33 34 Developmental plasticity-the environmentally induced phenotypic variance 35 associated with alternative developmental trajectories-has been proposed to fuel 36 adaptive evolution by initiating phenotypic changes (West-Eberhard 2005; Uller et al. 37 2018). Exploring the molecular mechanisms that underlie developmental plasticity can 38 reveal a direct link between environmental changes and phenotypic differentiation, 39 shedding light on how variation can surface from a single genotype in a stressful 40 environment. This knowledge has important consequences for current understanding 41 of evolutionary processes and human health (Lea et al. 2017b; Lea et al. 2017a). 42 Previous studies in flies, plants, fungi, and vertebrates suggest that 43 environmental changes that alter the molecular chaperone Hsp90's buffering capacity 44 during development can unlock cryptic genetic variation and boost phenotypic 45 diversification (Rutherford and Lindquist 1998; Queitsch et al. 2002; Yeyati et al. 46 2007; Jarosz and Lindquist 2010; Rohner et al. 2013). These observations 47 substantiate an evolutionary model where cryptic developmental variation, which is 48 revealed in response to environmental stress, might become genetically assimilated 49 (Waddington 1953). An alternative mechanism that links genetic and phenotypic 50 variation via environmental stress has also been proposed. Recent studies in flies 51 suggest that environmental stress, rather than exposing cryptic variation, may induce 52 de novo mutations, DNA deletions and transposon insertions (Fanti et al. 2017), 53 which can result from the disruption of a class of germline-specific small RNAs known 54 as Piwi-interacting RNAs (Specchia et al. 2010; Gangaraju et al. 2011). Following 55 stress-induced epigenetic changes, transposon activation or DNA deletions would 56 generate somatic changes, which might ultimately become heritable via de novo 57 germline ...

Environmentally induced nonrandom genomic changes 17 2 ABSTRACT 18 Long-term environmental exposure under selection-free conditions has 19 no consequences for fitness under the neo-Darwinian paradigm but it may 20 provoke adaptive developmental buffering if environmental pressures foster 21 directional organismal changes. To test this hypothesis, we revisited a 22