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Astatotilapia Burtoni Sex Differences in a Novel Object Recognition

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Astatotilapia Burtoni Sex Differences in a Novel Object Recognition bioRxiv preprint doi: https://doi.org/10.1101/2020.08.03.234658; this version posted October 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Equal performance but distinct behaviors: Astatotilapia burtoni sex differences in 2 a novel object recognition task and spatial maze 3 4 Kelly J. Wallace1 & Hans A. Hofmann1 5 1Department of Integrative Biology, University of Texas, Austin, TX, 78712, USA 6 Article Type: Research Article 7 8 Kelly J. Wallace ORCID: 0000-0002-2361-1213 9 Hans A. Hofmann ORCID: 0000-0002-3335-330X 10 11 Author for correspondence: Kelly J. Wallace 12 [email protected] 13 University of Texas at Austin, Department of Integrative Biology 14 1 University Station C0990 15 Austin, Texas 78712 16 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.03.234658; this version posted October 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 17 Highlights 18 - To ask if sexual dimorphism in cognition is reduced in a species where both 19 sexes navigate highly fluctuating social environments, we assessed performance 20 and behavior of the cichlid fish Astatotilapia burtoni in a novel object recognition 21 task and a spatial maze. 22 - Both sexes exhibited a preference for the familiar object during a novel object 23 recognition task, with males exhibiting the preference early in the task, whereas 24 females exhibiting the preference late in the task. 25 - In the spatial task, females reached the learning criterion more often than 26 expected by chance, whereas males did not. Females exhibited significantly 27 longer decision latencies and quicker error correction in the spatial task, 28 suggesting a sex-specific speed-accuracy tradeoff. 29 - The sexes differ in behaviors related to neophobia, space use, and decision 30 latencies. 31 - A model selection analysis to predict sex finds that novel object recognition task 32 preference, approach, and interaction duration are the most important terms on 33 average. 34 35 Abstract 36 Sex differences in behavior and cognition can be driven by differential selection 37 pressures from the environment and in the underlying neuromolecular mechanisms of 38 decision-making. The highly social cichlid fish Astatotilapia burtoni exhibits dynamic and 39 complex social hierarchies, yet explicit cognitive testing (outside of social contexts) and 40 investigations of sex differences in cognition have yet to be fully explored. Here we 41 assessed male and female A. burtoni in two cognitive tasks: a novel object recognition 42 task and a spatial task. We hypothesized that males outperform females in a spatial 43 learning task and exhibit more neophilic/exploratory behavior in across both tasks. In 44 the present study we find that both sexes prefer the familiar object in a novel object 45 recognition task, but the time at which they exhibit this preference differs between the 46 sexes. Females more frequently learned the spatial task, exhibiting longer decision 47 latencies and quicker error correction, suggesting a potential speed-accuracy tradeoff. 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.03.234658; this version posted October 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 48 Furthermore, the sexes differ in space use in both tasks and in a principal component 49 analysis of the spatial task. A model selection analysis finds that preference, approach, 50 and interaction duration in the novel object recognition task that reach a threshold of 51 importance averaged across all models. This work highlights the need to explicitly test 52 for sex differences in cognition to better understand how individuals navigate dynamic 53 social environments. 54 55 Keywords 56 sex differences, spatial learning, novel object recognition, social behavior, Astatotilapia 57 burtoni 58 59 Introduction 60 For humans and non-human animals alike, navigating dynamic social environments is a 61 constant challenge (O'Connell & Hofmann 2011, Taborsky & Oliveira 2012). Individuals 62 must attend to changing signals and cues, remember stimuli and their valence, assess 63 risk, make inferences from often incomplete or ambiguous information, use and update 64 prior associations, and display socially appropriate behaviors in varied contexts 65 including mate choice (Phelps & Ophir 2009, White & Galef 1999, Hebets & Sullivan- 66 Beckers 2010), territorial/dominance aggression (Reichert & Quinn 2017, Bshary & 67 Brown 2014), social foraging (Rapaport & Brown 2008, Thornton & McAuliffe 2006), and 68 nest building (Keagy et al. 2011). 69 70 Males and females frequently make different decisions even within the same social 71 environment. Sex differences in cognition, “the mechanisms by which animals acquire, 72 process, store, and act on information from the environment” (Shettleworth 2010) have 73 been described across taxa (rodents: Orsini & Setlow 2017, Dalla & Shors 2009, Rice et 74 al. 2017, songbirds: Titulaer et al. 2012, lizards: Carazo et al. 2014, poeciliid fish: 75 Lucon-Xiccato & Bisazza 2017a,b, Wallace et al. 2020), although males and females do 76 not always differ in this regard (Lucon-Xiccato & Bisazza 2014 and 2016; Healy 1999, 77 Guillette et al. 2009, Etheredge et al. 2018). When present, sex differences in cognition 78 often arise from varying ecological demands and fitness benefits of cognitive abilities 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.03.234658; this version posted October 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 79 such as sexually divergent pressures related to dispersal, predation, and mate choice 80 (Watson & Platt 2008). For example, males and females can differ in foraging patterns 81 (mice: Maille & Schradin 2016, cormorants: Ishikawa & Watanuki 2002, sandperch 82 Sano 1993) and response to predation (poeciliid fish: Magurran & Seghers 1994, 83 Magurran & Nowak 1991). Cognition can additionally impact fitness via reproductive 84 performance directly, such as sexual display quality (e.g. aspects of song quality in 85 songbirds), (Smith et al 2015, Boogert et al. 2011, Farrell et al. 2011) mate preference, 86 (Shohet & Watt 2009, Branch et al. 2019) or responses to sexual conflict (Cummings 87 2018, Buechel et al. 2016). Furthermore, behavior and decision-making can vary along 88 many axes including time (seasonality: Clayton & Krebs 1995, Yaskin 2011), social 89 status (Stowe et al. 2007, Layton & Fulton 2014), satiety (Caraco 1981), reproductive 90 status (Lynch et al 2005), and social context (Rosati & Hare 2012). 91 92 Burton’s mouthbrooder cichlid, Astatotilapia burtoni, is a highly social east African 93 cichlid fish that provides a unique system in which to explore sex differences in 94 cognition in a temporally dynamic social system (Hofmann & Fernald 2001, Maruska & 95 Fernald 2018). In this species, both sexes have been shown to navigate socio- 96 ecological demands that fluctuate across time: males bidirectionally shift between a 97 dominant phenotype (colorful, aggressive, territorial) and a subordinate phenotype (drab 98 coloration, submissive, non-territorial) (Fernald & Hirata 1977, Burmeister et al 2005, 99 Maruska & Fernald 2010, Huffman et al 2012), and females can also form complex 100 social hierarchies and display remarkable behavioral plasticity across reproductive 101 states (Fernald & Hirata 1977, Kidd et al. 2013a, White et al. 1996, Renn et al. 2012, 102 Kidd et al. 2013 a,b). Successfully navigating these complex and ever-changing social 103 surroundings requires cognitive abilities such as transitive inference and cognitive 104 flexibility, (Fernald 2014, Alcazar et al. 2014, Grosenick et al. 2007, Desjardins. et al 105 2012, Weitekamp et al. 2017, Rodriguez-Santiago et al 2020). Furthermore, this species 106 has emerged as a model system for understanding the overlapping neurobiological 107 mechanisms of social behavior and decision-making (Hofmann 2003, O’Connell & 108 Hofmann 2012, Maruska & Fernald 2018). While cognition has been examined in 109 naturalistic communities of A. burtoni (see Wood et al. 2011, Rodriguez-Santiago et al 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.03.234658; this version posted October 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 110 2020), studies that assess cognitive performance independent of social context and 111 across the sexes are lacking. In the present study we compare the sexes in two 112 cognitive tasks to examine whether and how the social environment might influence 113 cognition outside of the fast-paced social lives of this species. Assessing cognition 114 outside of social context is critical for understanding how socioecological pressures 115 influence decision-making and behavior more generally independent of ongoing social 116 interactions. 117 118 In the present study, we investigated whether A. burtoni males and females differed in 119 cognition by assessing individuals in a novel object recognition task (NOR) and a spatial 120 task (SPA). Both tasks require learning - a change in cognitive state or behavior 121 resulting from prior experience (Shettleworth 2010, Staddon 1983, Domjan 2015)- and 122 test abilities that are relevant to A.
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