Tactical Tentacles: New Insights on the Processes of Sexual Selection Among the Cephalopoda

Morse, Peter; Huffard, Christine L.

doi:10.3389/fphys.2019.01035

Cited by 25 publications

(14 citation statements)

References 180 publications

(521 reference statements)

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“…Most species are short‐lived (lifespans typically shorter than two years) and have a single reproductive period in which eggs are laid in a single or several temporally finite instances (Rocha, Guerra, & González, 2001; Hanlon & Messenger, 2018). A combination of limited breeding periods, occasional post‐mating cannibalism, and a highly skewed operational sex ratio experienced by various species results in fierce mating competition (Moynihan & Rodaniche, 1982; Hanlon et al ., 2005: Hanlon & Forsythe, 2008; Morse & Huffard, 2019). These three pressures – increased predation, increased foraging challenges, and intense mating competition – are thought to have driven the behavioural flexibility observed in cephalopods (Hanlon & Messenger, 2018; Schnell & Clayton, 2019; Amodio et al ., 2019a, 2019b).…”

Section: Introductionmentioning

confidence: 99%

How intelligent is a cephalopod? Lessons from comparative cognition

et al. 2020

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The soft‐bodied cephalopods including octopus, cuttlefish, and squid are broadly considered to be the most cognitively advanced group of invertebrates. Previous research has demonstrated that these large‐brained molluscs possess a suite of cognitive attributes that are comparable to those found in some vertebrates, including highly developed perception, learning, and memory abilities. Cephalopods are also renowned for performing sophisticated feats of flexible behaviour, which have led to claims of complex cognition such as causal reasoning, future planning, and mental attribution. Hypotheses to explain why complex cognition might have emerged in cephalopods suggest that a combination of predation, foraging, and competitive pressures are likely to have driven cognitive complexity in this group of animals. Currently, it is difficult to gauge the extent to which cephalopod behaviours are underpinned by complex cognition because many of the recent claims are largely based on anecdotal evidence. In this review, we provide a general overview of cephalopod cognition with a particular focus on the cognitive attributes that are thought to be prerequisites for more complex cognitive abilities. We then discuss different types of behavioural flexibility exhibited by cephalopods and, using examples from other taxa, highlight that behavioural flexibility could be explained by putatively simpler mechanisms. Consequently, behavioural flexibility should not be used as evidence of complex cognition. Fortunately, the field of comparative cognition centres on designing methods to pinpoint the underlying mechanisms that drive behaviours. To illustrate the utility of the methods developed in comparative cognition research, we provide a series of experimental designs aimed at distinguishing between complex cognition and simpler alternative explanations. Finally, we discuss the advantages of using cephalopods to develop a more comprehensive reconstruction of cognitive evolution.

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Section: Introductionmentioning

confidence: 99%

How intelligent is a cephalopod? Lessons from comparative cognition

et al. 2020

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“…Male octopus mate "at a distance" to escape and avoid sexual cannibalism (Hanlon and Forsythe, 2008;Huffard and Bartick, 2015). Promiscuity, mating aggregations, and sperm competition are also behavioral adaptations related to sexual selection in cephalopods (Hall and Hanlon, 2002;Jantzen and Havenhand, 2003;Naud et al, 2004;Morse and Huffard, 2019). For instance, several investigations have shown that multiple paternity occurs in some species, such as Octopus minor (Bo et al, 2016), Octopus vulgaris (Quinteiro et al, 2011), and the cuttlefish Sepiella japonica (Liu et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Dynamic Courtship Signals and Mate Preferences in Sepia plangon

2020

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Communication in cuttlefish includes rapid changes in skin coloration and texture, body posture and movements, and potentially polarized signals. The dynamic displays are fundamental for mate choice and agonistic behavior. We analyzed the reproductive behavior of the mourning cuttlefish Sepia plangon in the laboratory. Mate preference was analyzed via choice assays ( n = 33) under three sex ratios, 1 male (M): 1 female (F), 2M:1F, and 1M:2F. We evaluated the effect of modifying polarized light from the arms stripes and ambient light with polarized and unpolarized barriers between the cuttlefish. Additionally, to assess whether a particular trait was a determinant for mating, we used 3D printed cuttlefish dummies. The dummies had different sets of visual signals: two sizes (60 or 90 mm mantle length), raised or dropped arms, high or low contrast body coloration, and polarized or unpolarized filters to simulate the arms stripes. Frequency and duration (s) of courtship displays, mating, and agonistic behaviors were analyzed with GLM and ANOVAs. The behaviors, body patterns, and their components were integrated into an ethogram to describe the reproductive behavior of S. plangon . We identified 18 body patterns, 57 body patterns components, and three reproductive behaviors (mating, courtship, and mate guarding). Only sex ratio had a significant effect on courtship frequency, and the male courtship success rate was 80%. Five small (ML < 80 mm) males showed the dual-lateral display to access mates while avoiding fights with large males; this behavior is characteristic of male “sneaker” cuttlefish. Winner males showed up to 17 body patterns and 33 components, whereas loser males only showed 12 patterns and 24 components. We identified 32 combinations of body patterns and components that tended to occur in a specific order and were relevant for mating success in males. Cuttlefish were visually aware of the 3D-printed dummies; however, they did not start mating or agonistic behavior toward the dummies. Our findings suggest that in S. plangon , the dynamic courtship displays with specific sequences of visual signals, and the sex ratio are critical for mate choice and mating success.

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“…Polyandry, sexual dimorphism and sexual selection have been described in several lineages of cephalopod molluscs and is widespread in this group (Mann, 1984; Hanlon and Messenger, 1996; Squires et al, 2012). Polyandrous behavior has been observed in female octopuses, potentially increasing post-mating sexual selection and driving the evolution of a myriad of sperm transfer strategies (e.g., male mounting female; Figure 1A; for other examples see Hanlon and Messenger, 1996; Cheng and Caldwell, 2000; Huffard et al, 2008; Gutierrez et al, 2012; Morse and Huffard, 2019). In all cases, male octopuses pack their sperm into spermatophores and transfer them to females by using a modified arm called hectocotylus.…”

Section: Introductionmentioning

confidence: 99%

Sexual Selection and the Evolution of Male Reproductive Traits in Benthic Octopuses

et al. 2019

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Competition between same-sex organisms, or intra-sexual selection, can occur before and after mating, and include processes such as sperm competition and cryptic female choice. One of the consequences of intra-sexual selection is that male reproductive traits tend to evolve and diverge at high rates. In benthic octopuses, females often mate with more than one male in a single reproductive event, opening the venue for intra-sexual selection at multiple levels. For instance, males transfer spermatophores through hectocotylus, and can remove the spermatophores left by other males. Considering the limited evidence on post-copula competition in benthic octopuses, and the potential to affect the evolution of reproductive traits within octopodids, we put this hypothesis to a test employing a phylogenetic comparative approach. We combined data on hectocotylized arm length (HAL), ligula length (LL), spermatophore length (SL) with a Bayesian molecular phylogeny of 87 species, to analyze how reproductive traits have diverged across lineages and covary with body size (mantle length; ML). First, additionally to ML, we estimated the phylogenetic signal (λ) and mode of evolution (κ) in each reproductive trait. Second, we performed phylogenetic regressions to quantify the association among reproductive traits and their co-variation with ML. This analysis allowed us to estimate the phenotypic change along a branch into the phylogeny, and whether selection may have played a role in the evolution and diversification of specific clades. Estimations of λ were always high (>0.75), indicating concordance between the traits and the topology of the phylogenetic tree. Low values of κ (<1.0) suggested that evolution depends on branch lengths. All reproductive traits exhibiting a positive relation with ML (β > 0.5 in all cases). Overall, evolutionary rate models applied to the SL-ML regression suggested that octopuses of the family Megaleledonidae have evolved larger spermatophores than expected for their size. The regression HAL-ML indicated that HAL was more variable in Megaleledonidae than in the remaining clades, suggesting that the high divergence across species within this group might partially reflect intra-sexual selection. These results support the hypothesis that, at least in some lineages, sexual selection may account for the divergence in reproductive traits of male octopuses.

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Tactical Tentacles: New Insights on the Processes of Sexual Selection Among the Cephalopoda

Cited by 25 publications

References 180 publications

How intelligent is a cephalopod? Lessons from comparative cognition

How intelligent is a cephalopod? Lessons from comparative cognition

Dynamic Courtship Signals and Mate Preferences in Sepia plangon

Sexual Selection and the Evolution of Male Reproductive Traits in Benthic Octopuses

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