Sex differences in the cognitive abilities of a sex-changing fish species Labroides dimidiatus

Abstract

Males and females of the same species are known to differ at least in some cognitive domains, but such differences are not systematic across species. As a consequence, it remains unclear whether reported differences generally reflect adaptive adjustments to diverging selective pressures, or whether differences are mere side products of physiological differences necessary for reproduction. Here, we show that sex differences in cognition occur even in a sex-changing species, a protogynous hermaphroditic species where all males have previously been females. We tested male and female cleaner fish Labroides dimidiatus in four cognitive tasks to evaluate their learning and inhibitory control abilities first in an abstract presentation of the tasks, then in more ecologically relevant contexts. The results showed that males were better learners than females in the two learning tasks (i.e. reversal learning as an abstract task and a food quantity assessment task as an ecologically relevant task). Conversely, females showed enhanced abilities compared with males in the abstract inhibitory control task (i.e. detour task); but both sexes performed equally in the ecologically relevant inhibitory control task (i.e. ‘audience effect’ task). Hence, sex-changing species may offer unique opportunities to study proximate and/or ultimate causes underlying sex differences in cognitive abilities.

No evidence for general intelligence in a fish

“…We focussed on females because of their higher abundance and to strengthen the power of our analyses by avoiding to add another factor to the analyses. However, we know that cleaner fish males outperform females in the reversal learning task, while females outperform males in the detour task (Triki & Bshary, 2021). Therefore, we predict that adding males would not change the outcome.…”

“…Cleaners show various evidence for inhibitory control by detouring around barriers to reach a food source (Triki & Bshary, 2021), delaying gratification in order to receive a higher reward (Aellen et al, 2021) and being able to feed against preference (Bshary & Grutter, 2005). Also, cleaners perform very well in reversal learning tasks (Salwiczek et al, 2012; Triki & Bshary, 2021), which is the standard test for cognitive flexibility and where performance correlates with brain size in primates (Deaner et al, 2007). Working memory, the third important executive function, has not yet been tested in cleaners, but it has been shown that cleaners have very good long‐term memory (Triki & Bshary, 2019) and remember the ‘where’ and ‘when’ of interactions with clients (Salwiczek & Bshary, 2011).…”

“…Furthermore, cleaners solve tasks that test for so‐called ‘executive functions’, which are a family of general‐purpose top‐down mental processes that modulate the operation of various cognitive subprocesses (Burkart et al, 2017; Diamond, 2013; Miyake et al, 2000). Cleaners show various evidence for inhibitory control by detouring around barriers to reach a food source (Triki & Bshary, 2021), delaying gratification in order to receive a higher reward (Aellen et al, 2021) and being able to feed against preference (Bshary & Grutter, 2005). Also, cleaners perform very well in reversal learning tasks (Salwiczek et al, 2012; Triki & Bshary, 2021), which is the standard test for cognitive flexibility and where performance correlates with brain size in primates (Deaner et al, 2007).…”

Neuro-molecular characterization of fish cleaning interactions

“…We selected a common Acanthurid species as client since they are one of the most frequent hosts for Labroides species in coral reefs [20]. We also selected female individuals to be consistent with past studies using L. dimidiatus as a model species and because gene functions may differ between sexes and can blur the analysis of molecular signals [26]. Fishes were habituated for 28 days to laboratory conditions.…”

Cognitive-Behavioral Divergence Is Greater Across Alternative Male Reproductive Phenotypes Than Between the Sexes in a Wild Wrasse

“…Cognitive scientists are becoming more and more aware that sexual selection has a role in driving differences between the sexes in cognitive traits and the behaviors associated with them. Across a wide-range of taxa, studies have found significant differences in females' and males' spatial cognitive abilities (Jones et al, 2003;Jonasson, 2005;Carazo et al, 2014;Lucon-Xiccato and Bisazza, 2017), reversal learning abilities (Lucon-Xiccato and Bisazza, 2014;Fuss and Witte, 2019;Triki and Bshary, 2021), problem-solving and innovation (Laland and Reader, 1999;Aplin et al, 2013), and ability to recognize a spatial-temporal pattern (Wallace et al, 2020). It is important to note that in many cases there is no sexual dimorphism in cognitive performance (Healy et al, 1999;Lucon-Xiccato and Bisazza, 2016), and the difficulty of ensuring equal motivation between the sexes in cognition tasks can be daunting (Rowe and Healy, 2014).…”