Loss of heat acclimation capacity could leave subterranean specialists highly sensitive to climate change

Abstract

Physiological traits are key in determining the vulnerability of narrow range, highly specialized animals to climate change. It is generally predicted that species from more stable environments possess lower thermal tolerance breadths and thermal plasticity than those from more variable habitats – the so‐called ‘climatic variability hypothesis’. However, evolutionary trade‐offs between thermal breadth and its plasticity are also seen in some taxa, and the evolution of thermal physiology remains poorly understood. Subterranean environments are excellent systems for exploring these issues, being characterized by stable climatic conditions, with environmental variability increasing predictably from deep to shallow habitats. Acclimation capacity will be fundamental in determining the sensitivity of subterranean species to climate change, since they have poor dispersal capacity and limited possibility to exploit thermally different microhabitats in the uniform cave environment. We assessed critical thermal maximum (CTmax) and short‐term heat acclimation capacity in three related beetles (Leiodidae: Leptodirini) with differing degrees of specialization to the subterranean environment (deep, shallow and facultatively subterranean, respectively) and therefore exposed to contrasting thermal variability in nature. Only the facultative subterranean species showed any acclimatory capacity, also having the highest CTmax across the taxa studied. However, this species might experience the highest thermal stress in its habitat under climate change. The studied subterranean specialists will be poorly able to cope physiologically with temperature increase, but in contrast exposed to lower magnitude and rate of warming. Our results fit the climatic variability hypothesis, suggesting that adaptation to cave conditions has selected against the retention of acclimation mechanisms. We show that the pathways that determine vulnerability of subterranean species to climate change depend on their degree of specialization to deep subterranean environments. This information, combined with evaluation of exposure to climatic changes at their present locations, is fundamental in identifying species or populations at greatest risk.

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

“…As subterranean dytiscids likely descended from only a handful of epigean lineages (Leijs et al, 2012), meaningful comparisons can be made between these taxa despite their distributions being geographically disjunct. A recent study showed that P. macrosturtensis has a reduced upper thermal tolerance (or critical thermal maximum, CT max ) of 38.3°C compared to other epigean dytiscids (42–44.5°C) (Jones et al, 2021), mirroring previous results for other cave beetle species (Pallarés et al, 2020). These results also suggest P. macrosturtensis is unlikely to reach its thermal critical maximum under current climate change predictions.…”

“…Given the reduced thermal tolerance of P. macrosturtensis , it remains to be seen if the species could tolerate such extremes in the long term. Indeed, even cave beetles considered stenothermal–those that are only capable of surviving within an extremely narrow temperature range–have retained the HSR (Pallarés et al, 2020), but nonetheless cannot survive at extreme temperatures for long periods (>7 days) compared to epigean relatives (Bernabò et al, 2011; Rizzo et al, 2015).…”

“…Accordingly, the calcretes these species inhabit are considered a top conservation priority for protection by the Commonwealth Scientific and Industrial Research Organisation (Healy, 2015). Such threats are of particular concern for obligate stygofaunal species given the data presented by Jones et al (2021) and, more broadly, the fact that the thermal critical maximum of subterranean beetle species is known to decrease with the degree of subterranean specialisation (Pallarés et al, 2020). An increased knowledge of the assumed fragility of Australian subterranean dytiscids in the face of these stressors is therefore crucial for informing future conservation decisions.…”

Smelling in the dark: Phylogenomic insights into the chemosensory system of a subterranean beetle

“…33 Ma (Ribera et al, 2010)) acquired morphological and physiological traits typically associated with troglobitic adaptations. Their modifications include complete lack of eyes and optic lobes, depigmentation, membranous wings, elongation of antennae and legs (Deleurance, 1963; Jeannel, 1924; Luo et al, 2019) and loss of thermal acclimation capacity (Pallarés et al, 2020; Rizzo et al, 2015). They also exhibit modified life cycles as a key innovation for their subterranean specialization (Cieslak et al, 2014; Delay, 1978).…”

Additive effects of developmental acclimation and physiological syndromes on lifetime metabolic and water loss rates of a dry‐skinned ectotherm

“…Irreversible acclimation responses to developmental conditions might lead to maladaptive mismatches between the phenotype and ecological conditions in highly variable and unpredictable environments (Gluckman et al., 2007; Piersma & van Gils, 2011). Therefore, the ability of organisms to flexibly adjust their phenotype to environmental variations throughout their lifetime may determine their capacity to cope with climate change (Morley et al., 2019; Pallarés et al., 2020). Similarly, whether plastic responses supersede fixed inter‐individual differences in physiology has been poorly investigated so far, despite evidence of consistent physiological syndromes in some ectotherms (Goulet, Thompson, & Chapple, 2017; Mell et al., 2016).…”