Temperature-dependent life history and transcriptomic responses in heat-tolerant versus heat-sensitive Brachionus rotifers

Abstract

Thermal stress response is an essential physiological trait that determines occurrence and temporal succession in nature, including response to climate change. We compared temperature-related demography in closely related heat-tolerant and heat-sensitive Brachionus rotifer species. We found significant differences in heat response, with the heat-sensitive species adopting a strategy of long survival and low population growth, while the heat-tolerant followed the opposite strategy. In both species, we examined the genetic basis of physiological variation by comparing gene expression across increasing temperatures. Comparative transcriptomic analyses identified shared and opposing responses to heat. Interestingly, expression of heat shock proteins ( hsps ) was strikingly different in the two species and mirrored differences in population growth rates, showing that hsp genes are likely a key component of a species’ adaptation to different temperatures. Temperature induction caused opposing patterns of expression in further functional categories including energy, carbohydrate and lipid metabolism, and in genes related to ribosomal proteins. In the heat-sensitive species, elevated temperatures caused up-regulation of genes related to meiosis induction and post-translational histone modifications. This work demonstrates the sweeping reorganizations of biological functions that accompany temperature adaptation in these two species and reveals potential molecular mechanisms that might be activated for adaptation to global warming.

Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

“…Our molecular data mirrors previously documented reduced thermal tolerances in subterranean insects such as P. macrosturtensis . The species differentially expressed far fewer genes in response to 35 °C relative to the 25 °C treatment compared to P. nigroadumbratus ; similarly reduced numbers of differentially expressed genes have also been associated with lower thermal tolerances in other organisms such as fish 62 , lizards 63 , rotifers 64 , red algae 65 , and plants 66 , 67 , though we note the inverse (or alternatively, no clear pattern) has been observed in a number of cases, potentially reflecting lower levels of stress as opposed to an inability to mount a HSR 68 , 69 .…”

Variation in heat shock protein 40 kDa relates to divergence in thermotolerance among cryptic rotifer species

“…HSP gene expression levels correlated with life history traits such that the upregulation of HSP gene expression consistently occurred when the population growth rate was low. The two species were found to exhibit optimal growth at a different temperature ( B. calyciflorus s.s. at 26 °C and B. fernandoi at 20/23 °C) and increased their HSP expression outside their optimal temperature range, demonstrating a stress response of the organisms when optimal growth was not feasible 35 . The pronounced fitness differences at different thermal conditions indicate underlying mechanisms of phenotypes’ responses to environmental conditions that allow them to occur in sympatry, but in different seasons of the year 31 , 35 .…”

“…Prior to its delimitation into four species, the Brachionus calyciflorus species complex had been studied with regard to molecular phylogeny 23 – 25 , co-existence 26 , life history characteristics 27 , phylogeography 28 , 29 , and reproductive isolation 28 – 30 . More recent studies, which have taken into account the new species classification, focus on ecological processes, e.g., niche differentiation 31 , life history traits 32 , adaptation and the underlying regulatory mechanisms 33 – 35 , as well as on the robustness of species boundaries through hybridisation experiments 6 , 7 . These studies are of great importance to understand not only how these species have diverged, but also which of their adaptations are critical for the co-existence or exclusion of certain species in a specific environment.…”

“…A previous lifetable experiment 36 has demonstrated diverging temperature optima between Brachionus calyciflorus s.s. (heat-tolerant) and Brachionus fernandoi (heat-sensitive). Comparison of transcriptome data from the heat-tolerant B. calyciflorus s.s. and the heat-sensitive B. fernandoi revealed differential expression of Heat Shock Protein (HSP) genes relative to temperature 35 . HSP gene expression levels correlated with life history traits such that the upregulation of HSP gene expression consistently occurred when the population growth rate was low.…”

Mitochondrial genomes of the freshwater monogonont rotifer Brachionus fernandoi and of two additional B. calyciflorus sensu stricto lineages from Germany and the USA (Rotifera, Brachionidae)

“…Raw data are permanently stored on the NCBI Short Read Archive (accession numbers SRR9040995-8 and SRR10426055-76; Paraskevopoulou et al. 2019 , 2020 ).…”