Transcriptional dynamics following freezing stress reveal selection for mechanisms of freeze tolerance at the poleward range margin in the cold water intertidal barnacleSemibalanus balanoides

Abstract

Transcriptional dynamics following freezing stress reveal selection for mechanisms of freeze 3 tolerance at the poleward range margin in the cold water intertidal barnacle Semibalanus 4 balanoides 5 6 Running title: Transcription following freezing in S. balanoides 7 Abstract 22The ability to survive freezing has repeatedly evolved across multiple phyla. This suggests that 23 the mechanisms of freeze tolerance must be readily evolvable from basal physiological traits. 24While several biochemical correlates to freeze tolerance have been described, the mechanism that 25 confers freeze tolerance is still not well understood. To understand both the basic biochemical 26 mechanisms of freeze tolerance as well as their role in local adaptation at the poleward range 27 edge, we conducted a transcriptomic study on two populations (one from the poleward range 28 margin in the White Sea, Russia, and one from the central coast of British Columbia, Canada) of 29 the cold water acorn barnacle Semibalanus balanoides on a time series following a freezing 30 event. We found that the British Columbia population (at the equatorward range margin) was 31 significantly less freeze tolerant than the White Sea population (at the poleward range margin). 32After assembling and annotating a de novo transcriptome for S. balanoides, we found that the 33 patterns of differential transcript expression following freezing were almost entirely non-34 overlapping between the two populations, with the White Sea population expressing a series of 35 heat shock proteins in response to freezing stress as well as several aquaporins, while the British 36 Columbia population expressed a series of proteases instead, indicating severe protein damage. 37 We found strong evidence of purifying selection on the significantly upregulated transcripts in 38 the White Sea population, suggesting local adaptation to freezing threat. Taken together, this 39 shows the importance of freeze tolerance to population survival at the poleward range margin, 40 and highlights the central roles of aquaporins and heat shock proteins to the trait of freeze 41 tolerance across taxa. 42

Latitudinal patterns in intertidal ecosystem structure in West Greenland suggest resilience to climate change

“…Arctic populations of Fucus spp. can survive extended exposure to sub‐zero air temperatures without injury (Parker 1960, Becker et al 2009), and M. edulis and S. balanoides can survive air temperatures below −10°C (Thyrring et al 2015b, Marshall et al 2018). Thus, local environmental conditions on scales relevant to the organisms do not induce any vertical changes in the presence of foundation species in north Greenland.…”

Latitudinal patterns in intertidal ecosystem structure in West Greenland suggest resilience to climate change

“…across the intertidal assemblage, have a strong recovery capacity as they are able to reproduce, grow and recolonize following physical disturbance by ice (Kiirikki & Ruuskanen, 1996; Ørberg et al, 2018). Moreover, recent studies have shown adaptation to local environmental conditions takes place in intertidal Arctic populations of barnacles ( S. balanoides ) (Marshall et al, 2018) and blue mussels ( M. edulis ) (Telesca et al, 2019; Thyrring et al, 2020a). Thus, West Greenland’s intertidal ecosystem seems resilient to gradual climate change, and it is likely that introduced species could pose a greater risk for intertidal assemblages than climate change as increased shipping and propagule transport with the Irminger current increase the potential for introduction of non-native species (Ingolfsson, 1992; Renaud et al, 2015).…”

“…across the intertidal assemblage, have a strong recovery capacity as they are able to reproduce, grow and recolonize following physical disturbance by ice (Kiirikki & Ruuskanen, 1996;Ørberg et al, 2018). Moreover, recent studies have shown adaptation to local environmental conditions takes place in intertidal Arctic populations of barnacles (S. balanoides) (Marshall et al, 2018) and blue mussels (M. edulis) (Telesca et al, 2019;Thyrring et al, 2020a).…”

Local cold adaption increases the thermal window of temperate mussels in the Arctic

“…For instance, having evolved in a constant cold environment, Antarctic benthos is highly stenothermal with a small thermal window and a poor capacity to acclimate to elevated temperatures (Peck et al ., 2014). In temperate species, thermal adaptation involves change in enzymatic activity and gene expression, resulting in a reduced upper thermal tolerance in high latitude populations (Sokolova and Pörtner, 2001; King et al ., 2018; Marshall et al ., 2018). Our study demonstrates a different response in M. edulis .…”

“…For example, increased haemolymph concentrations of calcium and taurine have together with anaerobic byproducts, such as strombine, been shown to protect membranes and increase freeze tolerance of intertidal bivalves (Murphy, 1977; Loomis et al ., 1988). Furthermore, polar organisms often have additional heat shock proteins (HSP) (Peck, 2016), and the HSP production is upregulated in cold-adapted populations of intertidal barnacles ( Semibalanus balanoides ) following exposure to low air temperatures (Marshall et al ., 2018). The role of HSP in freeze tolerance is poorly understood, yet these chaperones may protects cells from freeze induced cell destabilization and irreversible protein denaturation, and should be investigated further.…”