Wake-like skin patterning and neural activity during octopus sleep.

While sleeping, many vertebrate groups alternate between at least two sleep stages: rapid eye movement and slow wave sleep1-4, in part characterized by wake-like and synchronous brain activity, respectively. Here we delineate neural and behavioural correlates of two stages of sleep in octopuses, marine invertebrates that evolutionarily diverged from vertebrates roughly 550 million years ago (ref. 5) and have independently evolved large brains and behavioural sophistication. 'Quiet' sleep in octopuses is rhythmically interrupted by approximately 60-s bouts of pronounced body movements and rapid changes in skin patterning and texture6. We show that these bouts are homeostatically regulated, rapidly reversible and come with increased arousal threshold, representing a distinct 'active' sleep stage. Computational analysis of active sleep skin patterning reveals diverse dynamics through a set of patterns conserved across octopuses and strongly resembling those seen while awake. High-density electrophysiological recordings from the central brain reveal that the local field potential (LFP) activity during active sleep resembles that of waking. LFP activity differs across brain regions, with the strongest activity during active sleep seen in the superior frontal and vertical lobes, anatomically connected regions associated with learning and memory function7-10. During quiet sleep, these regions are relatively silent but generate LFP oscillations resembling mammalian sleep spindles11,12 in frequency and duration. The range of similarities with vertebrates indicates that aspects of two-stage sleep in octopuses may represent convergent features of complex cognition.

Squid adjust their body color according to substrate.

Coleoid cephalopods camouflage on timescales of seconds to match their visual surroundings. To date, studies of cephalopod camouflage-to-substrate have been focused primarily on benthic cuttlefish and octopus, because they are readily found sitting on the substrate. In contrast to benthic cephalopods, oval squid (Sepioteuthis lessoniana species complex) are semi-pelagic animals that spend most of their time in the water column. In this study, we demonstrate that in captivity, S. lessoniana Sp.2 (Shiro-ika, white-squid) from the Okinawa archipelago, Japan, adapts the coloration of their skin using their chromatophores according to the background substrate. We show that if the animal moves between substrates of different reflectivity, the body patterning is changed to match. Chromatophore matching to substrate has not been reported in any loliginid cephalopod under laboratory conditions. Adaptation of the chromatophore system to the bottom substrate in the laboratory is a novel experimental finding that establishes oval squid as laboratory model animals for further research on camouflage.

Reevaluating claims of ecological speciation in Halichoeres bivittatus.

Allopatry has traditionally been viewed as the primary driver of speciation in marine taxa, but the geography of the marine environment and the larval dispersal capabilities of many marine organisms render this view somewhat questionable. In marine fishes, one of the earliest and most highly cited empirical examples of ecological speciation with gene flow is the slippery dick wrasse, Halichoeres bivittatus. Evidence for this cryptic or incipient speciation event was primarily in the form of a deep divergence in a single mitochondrial locus between the northern and southern Gulf of Mexico, combined with a finding that these two haplotypes were associated with different habitat types ("tropical" vs. "subtropical") in the Florida Keys and Bermuda, where they overlap. Here, we examine habitat assortment in the Florida Keys using a broader sampling of populations and habitat types than were available for the original study. We find no evidence to support the claim that haplotype frequencies differ between habitat types, and little evidence to support any differences between populations in the Keys. These results undermine claims of ecological speciation with gene flow in Halichoeres bivittatus. Future claims of this type should be supported by multiple lines of evidence that illuminate potential mechanisms and allow researchers to rule out alternative explanations for spatial patterns of genetic differences.

Comparing the dietary niche overlap and ecomorphological differences between invasive Hemidactylus mabouia geckos and a native gecko competitor.

Hemidactylus mabouia is one of the most successful, widespread invasive reptile species and has become ubiquitous across tropical urban settings in the Western Hemisphere. Its ability to thrive in close proximity to humans has been linked to the rapid disappearance of native geckos. However, aspects of Hemidactylus mabouia natural history and ecomorphology, often assumed to be linked with this effect on native populations, remain understudied or untested. Here, we combine data from ∂15N and ∂13C stable isotopes, stomach contents, and morphometric analyses of traits associated with feeding and locomotion to test alternate hypotheses of displacement between H. mabouia and a native gecko, Phyllodactylus martini, on the island of Curaçao. We demonstrate substantial overlap of invertebrate prey resources between the species, with H. mabouia stomachs containing larger arthropod prey as well as vertebrate prey. We additionally show that H. mabouia possesses several morphological advantages, including larger sizes in feeding-associated traits and limb proportions that could offer a propulsive locomotor advantage on vertical surfaces. Together, these findings provide the first support for the hypotheses that invasive H. mabouia and native P. martini overlap in prey resources and that H. mabouia possess ecomorphological advantages over P. martini. This work provides critical context for follow-up studies of H. mabouia and P. martini natural history and direct behavioral experiments that may ultimately illuminate the mechanisms underlying displacement on this island and act as a potential model for other systems with Hemidactylus mabouia invasions.

Cyclic nature of the REM sleep-like state in the cuttlefish Sepia officinalis.

Sleep is a state of immobility characterized by three key criteria: an increased threshold of arousal, rapid reversal to an alert state and evidence of homeostatic 'rebound sleep' in which there is an increase in the time spent in this quiescent state following sleep deprivation. Common European cuttlefish, Sepia officinalis, show states of quiescence during which they meet the last two of these three criteria, yet also show spontaneous bursts of arm and eye movements that accompany rapid changes in chromatophore patterns in the skin. Here, we report that this rapid eye movement sleep-like (REMS-like) state is cyclic in nature. Iterations of the REMS-like state last 2.42±0.22 min (mean±s.e.m.) and alternate with 34.01±1.49 min of the quiescent sleep-like state for durations lasting 176.89±36.71 min. We found clear evidence that this REMS-like state (i) occurs in animals younger than previously reported; (ii) follows an ultradian pattern; (iii) includes intermittent dynamic chromatophore patterning, representing fragments of normal patterning seen in the waking state for a wide range of signaling and camouflage; and (iv) shows variability in the intensity of expression of these skin patterns between and within individuals. These data suggest that cephalopods, which are mollusks with an elaborate brain and complex behavior, possess a sleep-like state that resembles behaviorally the vertebrate REM sleep state, although the exact nature and mechanism of this form of sleep may differ from that of vertebrates.

Eyes Wide Shut: the impact of dim-light vision on neural investment in marine teleosts.

Understanding how organismal design evolves in response to environmental challenges is a central goal of evolutionary biology. In particular, assessing the extent to which environmental requirements drive general design features among distantly related groups is a major research question. The visual system is a critical sensory apparatus that evolves in response to changing light regimes. In vertebrates, the optic tectum is the primary visual processing centre of the brain and yet it is unclear how or whether this structure evolves while lineages adapt to changes in photic environment. On one hand, dim-light adaptation is associated with larger eyes and enhanced light-gathering power that could require larger information processing capacity. On the other hand, dim-light vision may evolve to maximize light sensitivity at the cost of acuity and colour sensitivity, which could require less processing power. Here, we use X-ray microtomography and phylogenetic comparative methods to examine the relationships between diel activity pattern, optic morphology, trophic guild and investment in the optic tectum across the largest radiation of vertebrates-teleost fishes. We find that despite driving the evolution of larger eyes, enhancement of the capacity for dim-light vision generally is accompanied by a decrease in investment in the optic tectum. These findings underscore the importance of considering diel activity patterns in comparative studies and demonstrate how vision plays a role in brain evolution, illuminating common design principles of the vertebrate visual system.

Testing ontogenetic patterns of sexual size dimorphism against expectations of the expensive tissue hypothesis, an intraspecific example using oyster toadfish (Opsanus tau).

Trade-offs associated with sexual size dimorphism (SSD) are well documented across the Tree of Life. However, studies of SSD often do not consider potential investment trade-offs between metabolically expensive structures under sexual selection and other morphological modules. Based on the expectations of the expensive tissue hypothesis, investment in one metabolically expensive structure should come at the direct cost of investment in another. Here, we examine allometric trends in the ontogeny of oyster toadfish (Opsanus tau) to test whether investment in structures known to have been influenced by strong sexual selection conform to these expectations. Despite recovering clear changes in the ontogeny of a sexually selected trait between males and females, we find no evidence for predicted ontogenetic trade-offs with metabolically expensive organs. Our results are part of a growing body of work demonstrating that increased investment in one structure does not necessarily drive a wholesale loss of mass in one or more organs.

Molecular phylogenetics of squirrelfishes and soldierfishes (Teleostei: Beryciformes: Holocentridae): reconciling more than 100 years of taxonomic confusion.

Squirrelfishes and soldierfishes (Holocentridae) are among the most conspicuous species in the nocturnal reef fish community. However, there is no clear consensus regarding their evolutionary relationships, which is reflected in a complicated taxonomic history. We collected DNA sequence data from multiple single copy nuclear genes and one mitochondrial gene sampled from over fifty percent of the recognized holocentrid species and infer the first species-level phylogeny of the Holocentridae. Our results strongly support the monophyly of the clades Myripristinae (soldierfishes) and Holocentrinae (squirrelfishes). The molecular phylogenies differ with regard to previous hypotheses of relationships within the Myriprisitinae, resolving a clade of cryptic reef associated and deep water non-reef dwelling lineages (Corniger+Plectrypops+Ostichthys) that is the sister lineage to a monophyletic Myripristis. Within Holocentrinae, Neoniphon and Sargocentron are strongly supported as paraphyletic, while Holocentrus is nested within Sargocentron. Using Bayesian ancestral state reconstruction methods, we demonstrate the taxonomically diagnostic characters for Neoniphon and Sargocentron likely represent character states with a complex evolutionary history that is not reflective of shared common ancestry. We propose a new classification for Holocentrinae, recognizing four lineages that are treated as genera: Sargocentron Fowler, 1904, Holocentrus Scopoli, 1777, Flameo Jordan and Evermann, 1898, and Neoniphon Castelnau, 1875.