The evolution of predator avoidance in cephalopods: A case of brain over brawn?

Abstract

Predation is a major evolutionary driver of animal adaptation. However, understanding of anti-predator evolution is biased toward vertebrate taxa. Cephalopoda, a class in the invertebrate phylum Mollusca, are known for their diverse anti-predator strategies, characterised by their behavioural flexibility. While ancestral cephalopods were protected by a hard outer shell, extant cephalopods have greatly reduced their reliance on physical defences. Instead, cephalopods have evolved highly developed senses to identify potential threats, cryptic skin patterns to avoid detection, startle responses to deter attack, and elaborate means of escape. While cephalopod anti-predator repertoires are relatively well described, their evolution, and the selective pressures that shaped them, have received much less attention. This is despite their potential relevance, in turn, to elucidate evolution of the remarkable cognitive abilities of cephalopods. Here, we review cephalopod anti-predator evolution, considering four key aspects: (i) shell reduction and loss; (ii) the skin patterning system; (iii) the ecological context accompanying the evolution of advanced cognit.ive abilities; (iv) why the evolutionary trajectory taken by cephalopods is so unique among invertebrates. In doing so, we consider the unique physiology of cephalopods and discuss how this may have constrained or aided the development of their anti-predator repertoire. In particular, cephalopods are poorly equipped to defend themselves physically and escape predation by fish, due to a lack of comparable weaponry or musculature. We argue that this may have selected for alternative forms of defence, driving an evolutionary trajectory favouring crypsis and complex behaviours, and the promotion of sensory and cognitive adaptations. Unravelling the complexities of cephalopod anti-predator evolution remains challenging. However, recent technological developments available for cephalopod field and laboratory studies, coupled with new genomic data and analysis approaches, offer great scope to generate novel insights.

Octospy: What Octopus insularis do in their dens

“…One of the most dramatic changes in the evolutionary history of the octopods and other coleoid cephalopods was the transition from a hard‐shelled ancestor to a mostly soft body. This left coleoids vulnerable to predation by fishes, a selective pressure which likely drove the development of alternative ways to evade these predators, including crypsis, advanced sensory abilities, and cognitive complexity (Amodio et al, 2019a, 2019b; Grasso & Basil, 2009; Jaitly et al, 2022). Among those octopods that have adopted a benthic lifestyle, many (if not most) utilize a crevice or hard object as a protected refuge (Hanlon & Messenger, 2018), commonly referred to as a “den.” But what do octopuses do in their dens?…”

Whales and cephalopods in a deep‐sea arms race

“…The evolution of cephalopod avoidance strategies is strongly rooted in their response to predominantly visual predators. Cephalopods have co‐existed with their main predators, fishes, for 530 million years (Jaitly et al 2022). The much more recent entry of mammals into the marine realm and ensuing evolution of predatory toothed whale echolocation (34 million years ago), created strongly different selective pressures on cephalopod adaptive strategies to avoid predation—this time by acoustic predators.…”

“…Cephalopods can sense vibrations using a system analogous to the lateral line system of fishes, and rely on advanced visual capabilities to detect their predators (Jaitly et al 2022). The unusually large eyes of giant squid allow detection of the bioluminescent trail stimulated by approaching whales (Nilsson et al 2012).…”

“…The absence of an external shell limits the capacity for physical confrontation. Instead, cephalopod primary defense is to avoid detection, through physical and behavioral crypsis (Jaitly et al 2022).…”

“…To hide in a featureless epipelagic and mesopelagic environment where some light still penetrates, some cephalopods use their mantle for cryptic cover (e.g., Japetella heathi and Onychoteuthis banksi ) (Zylinski and Johnsen 2011). They can effectively switch between varying degrees of mantle pigmentation, counterillumination, shape and sometimes transparency, to optimize their camouflage to fluctuating light conditions (reviewed in Jaitly et al 2022) and hide from visually attuned predators.…”