A Theoretical Comparison of Alternative Male Mating Strategies in Cephalopods and Fishes.

We used computer simulations of growth, mating and death of cephalopods and fishes to explore the effect of different life-history strategies on the relative prevalence of alternative male mating strategies. Specifically, we investigated the consequences of single or multiple matings per lifetime, mating strategy switching, cannibalism, resource stochasticity, and altruism towards relatives. We found that a combination of single (semelparous) matings, cannibalism and an absence of mating strategy changes in one lifetime led to a more strictly partitioned parameter space, with a reduced region where the two mating strategies co-exist in similar numbers. Explicitly including Hamilton's rule in simulations of the social system of a Cichlid led to an increase of dominant males, at the expense of both sneakers and dwarf males ("super-sneakers"). Our predictions provide general bounds on the viable ratios of alternative male mating strategies with different life-histories, and under possibly rapidly changing ecological situations.

The physical basis of mollusk shell chiral coiling.

Snails are model organisms for studying the genetic, molecular, and developmental bases of left-right asymmetry in Bilateria. However, the development of their typical helicospiral shell, present for the last 540 million years in environments as different as the abyss or our gardens, remains poorly understood. Conversely, ammonites typically have a bilaterally symmetric, planispiraly coiled shell, with only 1% of 3,000 genera displaying either a helicospiral or a meandering asymmetric shell. A comparative analysis suggests that the development of chiral shells in these mollusks is different and that, unlike snails, ammonites with asymmetric shells probably had a bilaterally symmetric body diagnostic of cephalopods. We propose a mathematical model for the growth of shells, taking into account the physical interaction during development between the soft mollusk body and its hard shell. Our model shows that a growth mismatch between the secreted shell tube and a bilaterally symmetric body in ammonites can generate mechanical forces that are balanced by a twist of the body, breaking shell symmetry. In gastropods, where a twist is intrinsic to the body, the same model predicts that helicospiral shells are the most likely shell forms. Our model explains a large diversity of forms and shows that, although molluscan shells are incrementally secreted at their opening, the path followed by the shell edge and the resulting form are partly governed by the mechanics of the body inside the shell, a perspective that explains many aspects of their development and evolution.

Biomechanics, motor control and dynamic models of the soft limbs of the octopus and other cephalopods.

Muscular hydrostats are organs composed entirely of packed arrays of incompressible muscles and lacking any skeletal support. Found in both vertebrates and invertebrates, they are of great interest for comparative biomechanics from engineering and evolutionary perspectives. The arms of cephalopods (e.g. octopus and squid) are particularly interesting muscular hydrostats because of their flexibility and ability to generate complex behaviors exploiting elaborate nervous systems. Several lines of evidence from octopus studies point to the use of both brain and arm-embedded motor control strategies that have evolved to simplify the complexities associated with the control of flexible and hyper-redundant limbs and bodies. Here, we review earlier and more recent experimental studies on octopus arm biomechanics and neural motor control. We review several dynamic models used to predict the kinematic characteristics of several basic motion primitives, noting the shortcomings of the current models in accounting for behavioral observations. We also discuss the significance of impedance (stiffness and viscosity) in controlling the octopus's motor behavior. These factors are considered in light of several new models of muscle biomechanics that could be used in future research to gain a better understanding of motor control in the octopus. There is also a need for updated models that encompass stiffness and viscosity for designing and controlling soft robotic arms. The field of soft robotics has boomed over the past 15 years and would benefit significantly from further progress in biomechanical and motor control studies on octopus and other muscular hydrostats.

Crystal growth kinetics as an architectural constraint on the evolution of molluscan shells.

Molluscan shells are a classic model system to study formation-structure-function relationships in biological materials and the process of biomineralized tissue morphogenesis. Typically, each shell consists of a number of highly mineralized ultrastructures, each characterized by a specific 3D mineral-organic architecture. Surprisingly, in some cases, despite the lack of a mutual biochemical toolkit for biomineralization or evidence of homology, shells from different independently evolved species contain similar ultrastructural motifs. In the present study, using a recently developed physical framework, which is based on an analogy to the process of directional solidification and simulated by phase-field modeling, we compare the process of ultrastructural morphogenesis of shells from 3 major molluscan classes: A bivalve Unio pictorum, a cephalopod Nautilus pompilius, and a gastropod Haliotis asinina We demonstrate that the fabrication of these tissues is guided by the organisms by regulating the chemical and physical boundary conditions that control the growth kinetics of the mineral phase. This biomineralization concept is postulated to act as an architectural constraint on the evolution of molluscan shells by defining a morphospace of possible shell ultrastructures that is bounded by the thermodynamics and kinetics of crystal growth.

Cephalopods: Ambassadors for rethinking cognition.

Traditional approaches in comparative cognition have a long history of focusing on a narrow range of vertebrate species. However, in recent years the range of model species has expanded. Despite this development, invertebrate taxa are still largely neglected in comparative cognition, which limits our ability to locate the origins of cognitive traits. The time has come to rethink cognition and develop a more comprehensive understanding of cognitive evolution by expanding comparative analyses to include a diverse range of invertebrate taxa. In this review, we contend that cephalopods are suitable ambassadors for rethinking cognition. Cephalopods have large complex brains, exhibit sophisticated behavioral traits, and increasing evidence suggests that they possess complex cognitive abilities once thought to be unique to large-brained vertebrates. Comparing cephalopods with vertebrates, whose cognition has evolved independently, provides prominent opportunities to circumvent current limitations in comparative cognition that have arisen from traditional vertebrate comparisons. Increased efforts in investigating the cognitive abilities of cephalopods have also led to important welfare-related improvements. These large-brained molluscs are paving the way for a more inclusive approach to investigating cognitive evolution that we hope will extend to other invertebrate taxa.

A phylogenetic approach to understand the evolution of reproduction in coleoid cephalopods.

A central question in the evolution of life-histories is whether organisms reproduce once or repeatedly. For cephalopods, the main differences between semelparous and iteroparous are based on ovulation pattern and spawning type. The different reproductive strategies in coleoid cephalopods could be related to the habitat in which the species dwell (coastal vs. oceanic) and/or to environmental forces, thus, both aspects should be quantitatively evaluated under an evolutionary perspective to reconstruct: (a) the ancestral ovulation type of coleoid cephalopods, and (b) the potential of correlated evolution between ovulation type versus habitat and environment. Ancestral states of ovulation type were estimated using stochastic mapping based on literature data (i.e. synchronous or asynchronous), and this information was combined with a new molecular phylogeny including 165 species. The evolutionary correlation between ovulation type, habitat, and environment was estimated by means of the Markov model comparing the rates of gain and loss. The estimates of ancestral states of ovulation type for coleoid cephalopods resulted in a high probability that Octopodiformes evolved from synchronous ovulation type, and Decapodiformes from asynchronous ovulation type. The three traits evaluated presented phylogenetic signal, although no correlation was found between habitat and ovulation type. Overall, species in stable environments showed a tendency towards synchronous ovulation type, while the asynchronous ovulation pattern was found more frequently in species that live in unstable environments, being this last trait also responsible for triggering the change of ovulation type in some species throughout evolution.

The ammonite septum is not an adaptation to deep water: re-evaluating a centuries-old idea.

The shells of ammonoid cephalopods are among the most recognizable fossils, whose fractally folded, internal walls (septa) have inspired many hypotheses on their adaptive value. The enduring explanation for their iterative evolution is that they strengthen the shell against pressure at increasing water depths. The fossil record does not definitively support this idea and much of the theoretical mechanical work behind it has suffered from inaccurate testing geometries and conflicting results. By using a different set of mathematical methods compared with previous studies, I generate a system of finite-element models that explore how different parameters affect the shell's response to water pressure. Increasing the number of initial folds of the septa ultimately has little to no effect on the resulting stress in the shell wall or the septum itself. The introduction of higher-order folds does reduce the tensile stress in the shell wall; however, this is coupled with a higher rate of increase of tensile stress in the septum itself. These results reveal that the increase in complexity should not be expected to have a significant effect on the shell's strength and suggests that the evolution of ammonitic septa does not reflect a persistent trend towards deeper-water habitats.

Krüppel-like factor/specificity protein evolution in the Spiralia and the implications for cephalopod visual system novelties.

The cephalopod visual system is an exquisite example of convergence in biological complexity. However, we have little understanding of the genetic and molecular mechanisms underpinning its elaboration. The generation of new genetic material is considered a significant contributor to the evolution of biological novelty. We sought to understand if this mechanism may be contributing to cephalopod-specific visual system novelties. Specifically, we identified duplications in the Krüppel-like factor/specificity protein (KLF/SP) sub-family of C2H2 zinc-finger transcription factors in the squid Doryteuthis pealeii. We cloned and analysed gene expression of the KLF/SP family, including two paralogs of the DpSP6-9 gene. These duplicates showed overlapping expression domains but one paralog showed unique expression in the developing squid lens, suggesting a neofunctionalization of DpSP6-9a. To better understand this neofunctionalization, we performed a thorough phylogenetic analysis of SP6-9 orthologues in the Spiralia. We find multiple duplications and losses of the SP6-9 gene throughout spiralian lineages and at least one cephalopod-specific duplication. This work supports the hypothesis that gene duplication and neofunctionalization contribute to novel traits like the cephalopod image-forming eye and to the diversity found within Spiralia.

Spectral discrimination in color blind animals via chromatic aberration and pupil shape.

We present a mechanism by which organisms with only a single photoreceptor, which have a monochromatic view of the world, can achieve color discrimination. An off-axis pupil and the principle of chromatic aberration (where different wavelengths come to focus at different distances behind a lens) can combine to provide "color-blind" animals with a way to distinguish colors. As a specific example, we constructed a computer model of the visual system of cephalopods (octopus, squid, and cuttlefish) that have a single unfiltered photoreceptor type. We compute a quantitative image quality budget for this visual system and show how chromatic blurring dominates the visual acuity in these animals in shallow water. We quantitatively show, through numerical simulations, how chromatic aberration can be exploited to obtain spectral information, especially through nonaxial pupils that are characteristic of coleoid cephalopods. We have also assessed the inherent ambiguity between range and color that is a consequence of the chromatic variation of best focus with wavelength. This proposed mechanism is consistent with the extensive suite of visual/behavioral and physiological data that has been obtained from cephalopod studies and offers a possible solution to the apparent paradox of vivid chromatic behaviors in color blind animals. Moreover, this proposed mechanism has potential applicability in organisms with limited photoreceptor complements, such as spiders and dolphins.

Cephalopod Susceptibility to Asphyxiation via Ocean Incalescence, Deoxygenation, and Acidification.

Squids are powerful swimmers with high metabolic rates despite constrained oxygen uptake and transport. They have evolved novel physiological strategies for survival in extreme environments that provide insight into their susceptibility to asphyxiation under anthropogenic ocean incalescence (warming), deoxygenation, and acidification. Plasticity of ecological and physiological traits, in conjunction with vertical and latitudinal mobility, may explain their evolutionary persistence and ensure their future survival.

Comparative visual ecology of cephalopods from different habitats.

Previous investigations of vision and visual pigment evolution in aquatic predators have focused on fish and crustaceans, generally ignoring the cephalopods. Since the first cephalopod opsin was sequenced in late 1980s, we now have data on over 50 cephalopod opsins, prompting this functional and phylogenetic examination. Much of this data does not specifically examine the visual pigment spectral absorbance position (λmax) relative to environment or lifestyle, and cephalopod opsin functional adaptation and visual ecology remain largely unknown. Here we introduce a new protocol for photoreceptor microspectrophotometry (MSP) that overcomes the difficulty of bleaching the bistable visual pigment and that reveals eight coastal coleoid cephalopods to be monochromatic with λmax varying from 484 to 505 nm. A combination of current MSP results, the λmax values previously characterized using cephalopod retinal extracts (467-500 nm) and the corresponding opsin phylogenetic tree were used for systematic comparisons with an end goal of examining the adaptations of coleoid visual pigments to different light environments. Spectral tuning shifts are described in response to different modes of life and light conditions. A new spectral tuning model suggests that nine amino acid substitution sites may determine the direction and the magnitude of spectral shifts.

Adult and offspring size in the ocean: a database of size metrics and conversion factors.

The purpose of this dataset was to compile adult and offspring size estimates for marine organisms. Adult and offspring size estimates of 408 species were compiled from the literature covering >17 orders of magnitude in body mass and including Cephalopoda (ink fish), Cnidaria ("jelly" fish), Crustaceans, Ctenophora (comb jellies), Elasmobranchii (cartilaginous fish), Mammalia (mammals), Sagittoidea (arrow worms) and Teleost (i.e., Actinopterygii, bony fish). Individual size estimates were converted to standardized size estimates (carbon weight, g) to allow for among-group comparisons. This required a number of size estimates to be converted and a compilation of conversion factors obtained from the literature are also presented.

A Brief Review of Cephalopod Behavioral Responses to Sound.

Sound is a widely available cue in aquatic environments and is used by many marine animals for vital behaviors. Most research has focused on marine vertebrates. Relatively little is known about sound detection in marine invertebrates despite their abundance and importance in marine environments. Cephalopods are a key taxon in many ecosystems, but their behavioral interactions relative to acoustic stimuli have seldom been studied. Here we review current knowledge regarding (1) the frequency ranges and sound levels that generate behavioral responses and (2) the types of behavioral responses and their biological relevance.

Egg boons: central components of marine fatty acid food webs.

Food web relationships are traditionally defined in terms of the flow of key elements, such as carbon, nitrogen, and phosphorus, and their role in limiting production. There is growing recognition that availability of important biomolecules, such as fatty acids, may exert controls on secondary production that are not easily explained by traditional element-oriented models. Essential fatty acids (EFAs) are required by most organisms for proper physiological function but are manufactured almost entirely by primary producers. Therefore, the flow of EFAs, especially docosahexaenoic acid (DHA), eicosapentaenoic acid (EPA), and arachidonic acid (ARA), through aquatic food webs is critical for ecosystem functioning. A meta-analysis of data on the EFA content of marine organisms reveals that individual eggs of marine animals have exceptionally high concentrations of EFAs, and that superabundances of eggs released in temporally and spatially discrete patches create rich, but temporary, nutritional resources for egg predators, called "egg boons." Mortality rates of fish eggs are disproportionately higher than animals of similar size, and those eggs are consumed by predators, both larger and smaller than the adults that produce the eggs. Thus, egg boons are a major trophic pathway through which EFAs are repackaged and redistributed, and they are among the few pathways that run counter to the main direction of trophic flow. Egg boons can transport EFAs across ecosystems through advection of patches of eggs and spawning migrations of adults. Recognizing the significance of egg boons to aquatic food webs reveals linkages and feedbacks between organisms and environments that have important implications for understanding how food webs vary in time and space. Examples are given of top-down, bottom-up, and lateral control mechanisms that could significantly alter food webs through their effects on eggs. Our results suggest that trophodynamic food web models should include EFAs generally, and egg production and egg EFA content in particular.

The vertical lobe of cephalopods: an attractive brain structure for understanding the evolution of advanced learning and memory systems.

In this review we show that the cephalopod vertical lobe (VL) provides a good system for assessing the level of evolutionary convergence of the function and organization of neuronal circuitry for mediating learning and memory in animals with complex behavior. The pioneering work of JZ Young described the morphological convergence of the VL with the mammalian hippocampus, cerebellum and the insect mushroom body. Studies in octopus and cuttlefish VL networks suggest evolutionary convergence into a universal organization of connectivity as a divergence-convergence ('fan-out fan-in') network with activity-dependent long-term plasticity mechanisms. Yet, these studies also show that the properties of the neurons, neurotransmitters, neuromodulators and mechanisms of long-term potentiation (LTP) induction and maintenance are highly variable among different species. This suggests that complex networks may have evolved independently multiple times and that even though memory and learning networks share similar organization and cellular processes, there are many molecular ways of constructing them.

Genetic identification of a rare record of Ommastrephes Bartramii (Cephalopoda: Ommastrephidae) from the Eastern Adriatic Sea.

The neon flying squid Ommastrephes bartramii Lesueur, 1821 belongs to the Ommastrephidae, Cephalopoda family. The family Ommastrephidae (Mollusca: Cephalopoda) includes many commercially important species, dispersed around the world. The Ommastrephidae family is conventionally divided into three subfamilies (Illicinae, Todarodinae, and Ommastrephinae). We report a specimen of neon flying squid caught in the winter 2013 at Luka Sipanska, Island of Sipan, Croatia and identified at the genetic level using the standard mitochondrial COI barcode region. This record represents the first genetic identification of a neon flying squid from the Adriatic Sea.

Let's go beyond taxonomy in diet description: testing a trait-based approach to prey-predator relationships.

Understanding 'Why a prey is a prey for a given predator?' can be facilitated through trait-based approaches that identify linkages between prey and predator morphological and ecological characteristics and highlight key functions involved in prey selection. Enhanced understanding of the functional relationships between predators and their prey is now essential to go beyond the traditional taxonomic framework of dietary studies and to improve our knowledge of ecosystem functioning for wildlife conservation and management. We test the relevance of a three-matrix approach in foraging ecology among a marine mammal community in the northeast Atlantic to identify the key functional traits shaping prey selection processes regardless of the taxonomy of both the predators and prey. Our study reveals that prey found in the diet of marine mammals possess functional traits which are directly and significantly linked to predator characteristics, allowing the establishment of a functional typology of marine mammal-prey relationships. We found prey selection of marine mammals was primarily shaped by physiological and morphological traits of both predators and prey, confirming that energetic costs of foraging strategies and muscular performance are major drivers of prey selection in marine mammals. We demonstrate that trait-based approaches can provide a new definition of the resource needs of predators. This framework can be used to anticipate bottom-up effects on marine predator population dynamics and to identify predators which are sensitive to the loss of key prey functional traits when prey availability is reduced.

Cephalopod culture: current status of main biological models and research priorities.

A recent revival in using cephalopods as experimental animals has rekindled interest in their biology and life cycles, information with direct applications also in the rapidly growing ornamental aquarium species trade and in commercial aquaculture production for human consumption. Cephalopods have high rates of growth and food conversion, which for aquaculture translates into short culture cycles, high ratios of production to biomass and high cost-effectiveness. However, at present, only small-scale culture is possible and only for a few species: the cuttlefish Sepia officinalis, the loliginid squid Sepioteuthis lessoniana and the octopuses Octopus maya and O. vulgaris. These four species are the focus of this chapter, the aims of which are as follows: (1) to provide an overview of the culture requirements of cephalopods, (2) to highlight the physical and nutritional requirements at each phase of the life cycle regarded as essential for successful full-scale culture and (3) to identify current limitations and the topics on which further research is required. Knowledge of cephalopod culture methods is advanced, but commercialization is still constrained by the highly selective feeding habits of cephalopods and their requirement for large quantities of high-quality (preferably live) feed, particularly in the early stages of development. Future research should focus on problems related to the consistent production of viable numbers of juveniles, the resolution of which requires a better understanding of nutrition at all phases of the life cycle and better broodstock management, particularly regarding developments in genetic selection, control of reproduction and quality of eggs and offspring.

Transitions during cephalopod life history: the role of habitat, environment, functional morphology and behaviour.

Cephalopod life cycles generally share a set of stages that take place in different habitats and are adapted to specific, though variable, environmental conditions. Throughout the lifespan, individuals undertake a series of brief transitions from one stage to the next. Four transitions were identified: fertilisation of eggs to their release from the female (1), from eggs to paralarvae (2), from paralarvae to subadults (3) and from subadults to adults (4). An analysis of each transition identified that the changes can be radical (i.e. involving a range of morphological, physiological and behavioural phenomena and shifts in habitats) and critical (i.e. depending on environmental conditions essential for cohort survival). This analysis underlines that transitions from eggs to paralarvae (2) and from paralarvae to subadults (3) present major risk of mortality, while changes in the other transitions can have evolutionary significance. This synthesis suggests that more accurate evaluation of the sensitivity of cephalopod populations to environmental variation could be achieved by taking into account the ontogeny of the organisms. The comparison of most described species advocates for studies linking development and ecology in this particular group.

The study of deep-sea cephalopods.

"Deep-sea" cephalopods are here defined as cephalopods that spend a significant part of their life cycles outside the euphotic zone. In this chapter, the state of knowledge in several aspects of deep-sea cephalopod research are summarized, including information sources for these animals, diversity and general biogeography and life cycles, including reproduction. Recommendations are made for addressing some of the remaining knowledge deficiencies using a variety of traditional and more recently developed methods. The types of oceanic gear that are suitable for collecting cephalopod specimens and images are reviewed. Many groups of deep-sea cephalopods require taxonomic reviews, ideally based on both morphological and molecular characters. Museum collections play a vital role in these revisions, and novel (molecular) techniques may facilitate new use of old museum specimens. Fundamental life-cycle parameters remain unknown for many species; techniques developed for neritic species that could potentially be applied to deep-sea cephalopods are discussed. Reproductive tactics and strategies in deep-sea cephalopods are very diverse and call for comparative evolutionary and experimental studies, but even in the twenty-first century, mature individuals are still unknown for many species. New insights into diet and trophic position have begun to reveal a more diverse range of feeding strategies than the typically voracious predatory lifestyle known for many cephalopods. Regular standardized deep-sea cephalopod surveys are necessary to provide insight into temporal changes in oceanic cephalopod populations and to forecast, verify and monitor the impacts of global marine changes and human impacts on these populations.