Behavioral Laterality and Morphological Asymmetry in the Cuttlefish, Sepia lycidas

Abstract

Behavioral laterality is widely found among vertebrates, but has been little studied in aquatic invertebrates. We examined behavioral laterality in attacks on prey shrimp by the cuttlefish, Sepia lycidas, and correlated this to their morphological asymmetry. Behavioral tests in the laboratory revealed significant individual bias for turning either clockwise or counterclockwise toward prey, suggesting behavioral dimorphism in foraging behavior. Morphological bias was examined by measuring the curvature of the cuttlebone; in some the cuttlebone was convex to the right (righty), while in others, the cuttlebone was convex to the left (lefty). The frequency distributions of an index of cuttlebone asymmetry were bimodal, indicating that populations were composed of two types of individuals: "righty" and "lefty." Moreover, an individual's laterality in foraging behavior corresponded with the asymmetry of its cuttlebone, with righty individuals tending to turn counterclockwise and lefty ones in the opposite direction. These results indicate that cuttlefish exhibit behavioral dimorphism and morphological antisymmetry in natural populations. The presence of two types of lateral morph in cuttlefish provides new information on the relationship between antisymmetric morphologies and the evolution of individual laterality in behavioral responses in cephalopods. The implications of these findings for the interpretation of ecological meaning and maintenance mechanisms of laterality in cuttlefish are also discussed.

Anticlockwise or clockwise? A dynamic Perception-Action-Laterality model for directionality bias in visuospatial functioning

“…For example, it has been shown that lateralized fish perform better than nonlateralized fish when they are tested for their ability to capture shrimp in the presence of a predator; however, such a difference was not observed in the absence of a predator (Dadda & Bisazza, 2006). Consistently and very interestingly, Lucky, Ihara, Yamaoka and Hori (2012) were the first to show directly the clockwise vs anticlockwise turning bias in young cuttlefishes ( Sepia lycidas ). In a laboratory experiment, they investigated laterality in attacks on shrimps by cuttlefishes, and correlated this with morphological asymmetry as measured by the curvature of cuttlebone.…”

“…Additionally, chicks hatched from eggs incubated in completely dark conditions do not develop any asymmetry in the visual pathways and visual behavior in categorization of food items and in responding to predators (Rogers, 2012). Light exposure during embryonic development also affects the development of lateralized behavior in zebrafish (Budaev & Andrew, 2009) and in cuttlefishes it is caused by morphological asymmetry of the cuttlebone (Lucky et al, 2012). However, we are not precluding the possible contributions of the general factors that may cause directionality bias in non-human animals as in humans.…”

“…Laterality of predatory behavior in cuttlefishes ( Sepia lycidas, from Lucky et al, 2012, with permission).…”

Left-handed sperm removal by male Calopteryx damselflies (Odonata)

“…Recent studies have highlighted the adaptive significance of asymmetric organs and their consequent behaviours; for example, laterally biased male-male fighting in fish (Takeuchi et al 2010), left/right-handed scale-eating in fish (Hori 1993), right-handed snail-eating in snakes (Hoso et al 2007) and in larval water beetles (Inoda et al 2003), and left/rightward predator-avoiding jumping in shrimp (Takeuchi et al 2008), crayfish (Tobo et al 2012) and cuttlefish (Lucky et al 2012). Insects are the most divergent animal group and their taxonomic literature has provided details on many cases of asymmetric genitalia (reviewed by Huber et al 2007;Schilthuizen 2013).…”

Gene(s) and individual feeding behavior: Exploring eco‐evolutionary dynamics underlying left‐right asymmetry in the scale‐eating cichlid fishPerissodus microlepis

“…Stable polymorphisms such as conspicuous asymmetry (departure from symmetry in morphology) or handedness (lateralized behavior) have repeatedly emerged in both vertebrates and invertebrates (Ludwig, 1932; Palmer, 2004, 2009, 2016; e.g., Hori, 1993; Kurvers et al., 2017; Lucky, Ihara, Yamaoka, & Hori, 2012; Matsui, Takeuchi, & Hori, 2013; Takeuchi & Hori, 2008; Tobo, Takeuchi, & Hori, 2012). Yet, the evolutionary forces and the underlying genetic and developmental mechanisms underpinning most of these stable asymmetries (i.e., excluding fluctuating asymmetries) remain unclear (Palmer, 2016; Uzoigwe, 2013).…”