Short telomeres drive pessimistic judgement bias in zebrafish

Abstract

The role of telomerase reverse transcriptase has been widely investigated in the contexts of ageing and age-related diseases. Interestingly, decreased telomerase activities (and accelerated telomere shortening) have also been reported in patients with emotion-related disorders, opening the possibility for subjective appraisal of stressful stimuli playing a key role in stress-driven telomere shortening. In fact, patients showing a pessimistic judgement bias have shorter telomeres. However, in humans the evidence for this is correlational and the causal directionality between pessimism and telomere shortening has not been established experimentally yet. We have developed and validated a judgement bias experimental paradigm to measure subjective evaluations of ambiguous stimuli in zebrafish. This behavioural assay allows classification of individuals in an optimistic–pessimistic dimension (i.e. from individuals that consistently evaluate ambiguous stimuli as negative to others that perceive them as positive). Using this behavioural paradigm we found that telomerase-deficient zebrafish ( tert − / − ) were more pessimistic in response to ambiguous stimuli than wild-type zebrafish. The fact that individuals with constitutive shorter telomeres have pessimistic behaviours demonstrates for the first time in a vertebrate model a genetic basis of judgement bias.

Causes and consequences of variation in early‐life telomere length in a bird metapopulation

“…Other explanations may underlie this observation, including TL being affected by environmental factors that also induce dispersal (e.g., habitat quality, Wilbourn et al, 2017 ), or influences individual quality. However, short telomeres have been correlated with bold, aggressive, pessimistic, or impulsive behavior in fish and birds (Adriaenssens et al, 2016 ; Bateson et al, 2015 ; Espigares et al, 2021 ). Increases in the level of glucocorticoids are linked to dispersal in birds (Belthoff & Dufty, 1998 ; Récapet et al, 2016 ; Silverin, 1997 ), but although Pegan et al ( 2019 ) found a small negative effect of corticosterone treatment on TL in wild tree swallows ( Tachycineta bicolor ), this did not affect the age of initial departure from the natal site.…”

“…Giraudeau, Angelier, and Sepp ( 2019 ) speculated that TL could act as a physiological mediator of the individual variation in suites of life‐history traits (pace‐of‐life syndromes, e.g., Reale et al, 2010 ) within species. It has also been suggested that telomere dynamics may underlie behavioral patterns or personalities (Adriaenssens et al, 2016 ; Bateson & Nettle, 2018 ; Espigares et al, 2021 ). However, studies have yet to identify the mechanisms underlying TL dynamics in natural populations and the potential of using TL as a biomarker of physiological costs of individual experiences, or somatic redundancy, in the wild (Bateson & Poirier, 2019 ; Boonekamp et al, 2013 ).…”

Research Before Policy: Identifying Gaps in Salmonid Welfare Research That Require Further Study to Inform Evidence-Based Aquaculture Guidelines in Canada

“…For example, a judgment bias task was recently validated for laboratory mice, wherein mice housed with preferred and welfareimproving environmental enrichment and tumor-bearing nude mice showed optimistic and pessimistic responses, respectively (196). Judgment bias tasks have been attempted for zebrafish [e.g., (197)], but a validated method for salmonids has yet to emerge.…”

Neuromolecular Underpinnings of Negative Cognitive Bias in Depression

“…Nonetheless, research on the genetic background of judgment bias is still scarce. In a recent study using the ACI paradigm in zebrafish, Espigares and colleagues found that telomerase-deficient fish (tert−/−) were more pessimistic in response to ambiguous stimuli than their wild-type conspecifics [53]. These telomerase-deficient mutants have shorter telomeres than their wild-type siblings and develop degenerative phenotypes characterized by, e.g., increased inflammation, which is common in aged organisms.…”