A morphological basis for path-dependent evolution of visual systems.

Path dependence influences macroevolutionary predictability by constraining potential outcomes after critical evolutionary junctions. Although it has been demonstrated in laboratory experiments, path dependence is difficult to demonstrate in natural systems because of a lack of independent replicates. Here, we show that two types of distributed visual systems recently evolved twice within chitons, demonstrating rapid and path-dependent evolution of a complex trait. The type of visual system that a chiton lineage can evolve is constrained by the number of openings for sensory nerves in its shell plates. Lineages with more openings evolve visual systems with thousands of eyespots, whereas those with fewer openings evolve visual systems with hundreds of shell eyes. These macroevolutionary outcomes shaped by path dependence are both deterministic and stochastic because possibilities are restricted yet not entirely predictable.

HES and Mox genes are expressed during early mesoderm formation in a mollusk with putative ancestral features.

The mesoderm is considered the youngest of the three germ layers. Although its morphogenesis has been studied in some metazoans, the molecular components underlying this process remain obscure for numerous phyla including the highly diverse Mollusca. Here, expression of Hairy and enhancer of split (HES), Mox, and myosin heavy chain (MHC) was investigated in Acanthochitona fascicularis, a representative of Polyplacophora with putative ancestral molluscan features. While AfaMHC is expressed throughout myogenesis, AfaMox1 is only expressed during early stages of mesodermal band formation and in the ventrolateral muscle, an autapomorphy of the polyplacophoran trochophore. Comparing our findings to previously published data across Metazoa reveals Mox expression in the mesoderm in numerous bilaterians including gastropods, polychaetes, and brachiopods. It is also involved in myogenesis in molluscs, annelids, tunicates, and craniates, suggesting a dual role of Mox in mesoderm and muscle formation in the last common bilaterian ancestor. AfaHESC2 is expressed in the ectoderm of the polyplacophoran gastrula and later in the mesodermal bands and in putative neural tissue, whereas AfaHESC7 is expressed in the trochoblasts of the gastrula and during foregut formation. This confirms the high developmental variability of HES gene expression and demonstrates that Mox and HES genes are pleiotropic.

Arctic coastal benthos long-term responses to perturbations under climate warming.

Climate warming influences structure and function of Arctic benthic ecosystems. Assessing the response of these systems to perturbations requires long-term studies addressing key ecological processes related to recolonization and succession of species. Based on unique time-series (1980-2017), this study addresses successional patterns of hard-bottom benthos in two fjords in NW Svalbard after a pulse perturbation in 1980 and during a period of rapid climate warming. Analysis of seafloor photographs revealed different return rates of taxa, and variability in species densities, through time. It took 13 and 24 years for the community compositions of cleared and control transects to converge in the two fjords. Nearly two decades after the study initiation, an increase in filamentous and foliose macroalgae was observed with a subsequent reorganization in the invertebrate community. Trait analyses showed a decrease in body size and longevity of taxa in response to the pulse perturbation and a shift towards small/medium size and intermediate longevity following the macroalgae takeover. The observed slow recovery rates and abrupt shifts in community structure document the vulnerability of Arctic coastal ecosystems to perturbations and continued effects of climate warming. This article is part of the theme issue 'The changing Arctic Ocean: consequences for biological communities, biogeochemical processes and ecosystem functioning'.

Dorsoventral decoupling of Hox gene expression underpins the diversification of molluscs.

In contrast to the Hox genes in arthropods and vertebrates, those in molluscs show diverse expression patterns with differences reported among lineages. Here, we investigate 2 phylogenetically distant molluscs, a gastropod and a polyplacophoran, and show that the Hox expression in both species can be divided into 2 categories. The Hox expression in the ventral ectoderm generally shows a canonical staggered pattern comparable to the patterns of other bilaterians and likely contributes to ventral patterning, such as neurogenesis. The other category of Hox expression on the dorsal side is strongly correlated with shell formation and exhibits lineage-specific characteristics in each class of mollusc. This generalized model of decoupled dorsoventral Hox expression is compatible with known Hox expression data from other molluscan lineages and may represent a key characteristic of molluscan Hox expression. These results support the concept of widespread staggered Hox expression in Mollusca and reveal aspects that may be related to the evolutionary diversification of molluscs. We propose that dorsoventral decoupling of Hox expression allowed lineage-specific dorsal and ventral patterning, which may have facilitated the evolution of diverse body plans in different molluscan lineages.

Shallow and deep-sea chitons of the genus Leptochiton Gray, 1847 (Mollusca: Polyplacophora: Lepidopleurida) from Peruvian and Chilean waters.

The Southeast region off Chile and Peru has yielded a very rich diverse fauna of basal chitons of the genus Leptochiton. The present contribution is based on the study of 1055 specimens of chitons. Thirteen leptochitonid species are reported of which seven species are new, namely Leptochiton lascrusesi n. sp., L. linseae n. sp., L. longibranchiae n. sp., L. peruvianus n. sp., L. macleani n. sp., L. sigwartae n. sp., and L. mutschkeae n. sp. Five species were found on the shelf, but only one of those is limited to this zone. The other eight species live in bathyal or abyssal depths. Thus, 12 of 13 species were found deeper than 200 m. The genus Leptochiton originated in the late Palaeozoic in shallow waters. It probably shifted to deep-waters because of competition by more advanced genera of chitons. The leptochitonid fauna of the Peru-Chile Trench turned out to be rich. Five species were studied from this trench system. Two of them-L. longibranchiae n. sp. and L. peruvianus n. sp.-are characterized by an unusually high number of gills and an accordingly wider distribution in the mantle cavity, reaching in an anterior direction to valves V and III. This morphological peculiarity is unusual for Lepidopleurida and resembles the conditions found in the order Chitonida.

Is the Schwabe Organ a Retained Larval Eye? Anatomical and Behavioural Studies of a Novel Sense Organ in Adult Leptochiton asellus (Mollusca, Polyplacophora) Indicate Links to Larval Photoreceptors.

The discovery of a sensory organ, the Schwabe organ, was recently reported as a unifying feature of chitons in the order Lepidopleurida. It is a patch of pigmented tissue located on the roof of the pallial cavity, beneath the velum on either side of the mouth. The epithelium is densely innervated and contains two types of potential sensory cells. As the function of the Schwabe organ remains unknown, we have taken a cross-disciplinary approach, using anatomical, histological and behavioural techniques to understand it. In general, the pigmentation that characterises this sensory structure gradually fades after death; however, one particular concentrated pigment dot persists. This dot is positionally homologous to the larval eye in chiton trochophores, found in the same neuroanatomical location, and furthermore the metamorphic migration of the larval eye is ventral in species known to possess Schwabe organs. Here we report the presence of a discrete subsurface epithelial structure in the region of the Schwabe organ in Leptochiton asellus that histologically resembles the chiton larval eye. Behavioural experiments demonstrate that Leptochiton asellus with intact Schwabe organs actively avoid an upwelling light source, while Leptochiton asellus with surgically ablated Schwabe organs and a control species lacking the organ (members of the other extant order, Chitonida) do not (Kruskal-Wallis, H = 24.82, df = 3, p < 0.0001). We propose that the Schwabe organ represents the adult expression of the chiton larval eye, being retained and elaborated in adult lepidopleurans.

A new name for the deep-sea chiton Leptochiton clarki Sigwart & Sirenko non Berry (Lepidopleurida: Leptochitonidae).

Recently we described several new species of chitons living in deep water deposits of sunken wood in the southwest Pacific (Sigwart & Sirenko 2012). Among these, one species, Leptochiton clarki Sigwart & Sirenko, 2012, is homonymous with a fossil taxon of the same genus: Leptochiton clarki Berry, 1922. Herein, we replace this homonym with a new name according to International Code of Zoological Nomenclature (ICZN 1999: Art. 57.2).

Emergence, development, and maturity of the gonad of two species of chitons "sea cockroach" (Mollusca: Polyplacophora) through the early life stages.

This study describes and recognises, using histological and microscopical examinations on a morphometrical basis, several gonad traits through the early life stages of Chiton articulatus and C. albolineatus. Gonadal ontogenesis, gonad development stages, sexual differentiation, onset of the first sexual maturity, and growth sequences or "early life stages" were determined. In addition, allometry between lengths and body weight pooled for both sexes per each chiton were calculated using equation Y = aX(b) . A total of 125 chitons (4≤TL≤40 mm, in total length "TL") were used. All allometric relations showed a strong positive correlation (r), close to 1, with b-values above three, indicating an isometric growth. Gonadal ontogenesis and gonad development stages were categorised into three periods ("Pw" without gonad, "Pe" gonad emergence, and "Pf" gonadal sac formed) and four stages ("S0" gametocytogenesis, "S1" gametogenesis, "S2" mature, and "S3" spawning), respectively. Compound digital images were attained for each process. Periods and stages are overlapped among them and between species, with the following overall confidence intervals in TL: Pw 6.13-14.32 mm, Pe 10.32-16.93 mm, Pf 12.99-25.01 mm, S0 16.08-24.34 mm (females) and 19.51-26.60 mm (males), S1 27.15-35.63 mm (females) and 23.45-32.27 mm (males), S2 24.48-40.24 mm (females) and 25.45-32.87 mm (males). Sexual differentiation (in S0) of both chitons occurs first as a female then as a male; although, males reach the onset of the first sexual maturity earlier than females, thus for C. articulatus males at 17 mm and females at 32 mm, and for C. albolineatus males at 23.5 mm and females at 28 mm, all in TL. Four early life stages (i.e., subjuvenile, juvenile, subadult, and adult) are described and proposed to distinguish growth sequences. Our results may be useful to diverse disciplines, from developmental biology to fisheries management.

Larval transport modeling of deep-sea invertebrates can aid the search for undiscovered populations.

BACKGROUND: Many deep-sea benthic animals occur in patchy distributions separated by thousands of kilometres, yet because deep-sea habitats are remote, little is known about their larval dispersal. Our novel method simulates dispersal by combining data from the Argo array of autonomous oceanographic probes, deep-sea ecological surveys, and comparative invertebrate physiology. The predicted particle tracks allow quantitative, testable predictions about the dispersal of benthic invertebrate larvae in the south-west Pacific. PRINCIPAL FINDINGS: In a test case presented here, using non-feeding, non-swimming (lecithotrophic trochophore) larvae of polyplacophoran molluscs (chitons), we show that the likely dispersal pathways in a single generation are significantly shorter than the distances between the three known population centres in our study region. The large-scale density of chiton populations throughout our study region is potentially much greater than present survey data suggest, with intermediate 'stepping stone' populations yet to be discovered. CONCLUSIONS/SIGNIFICANCE: We present a new method that is broadly applicable to studies of the dispersal of deep-sea organisms. This test case demonstrates the power and potential applications of our new method, in generating quantitative, testable hypotheses at multiple levels to solve the mismatch between observed and expected distributions: probabilistic predictions of locations of intermediate populations, potential alternative dispersal mechanisms, and expected population genetic structure. The global Argo data have never previously been used to address benthic biology, and our method can be applied to any non-swimming larvae of the deep-sea, giving information upon dispersal corridors and population densities in habitats that remain intrinsically difficult to assess.

Ultrastructure of the epithelial cells associated with tooth biomineralization in the chiton Acanthopleura hirtosa.

The cusp epithelium is a specialized branch of the superior epithelium that surrounds the developing teeth of chitons and is responsible for delivering the elements required for the formation of biominerals within the major lateral teeth. These biominerals are deposited within specific regions of the tooth in sequence, making it possible to conduct a row by row examination of cell development in the cusp epithelium as the teeth progress from the unmineralized to the mineralized state. Cusp epithelium from the chiton Acanthopleura hirtosa was prepared using conventional chemical and microwave assisted tissue processing, for observation by light microscopy, conventional transmission electron microscopy (TEM) and energy filtered TEM. The onset of iron mineralization within the teeth, initiated at row 13, is associated with a number of dramatic changes in the ultrastructure of the apical cusp cell epithelium. Specifically, the presence of ferritin containing siderosomes, the position and number of mitochondria, and the structure of the cell microvilli are each linked to aspects of the mineralization process. These changes in tissue development are discussed in context with their influence over the physiological conditions within both the cells and extracellular compartment of the tooth at the onset of iron mineralization.

The chiton stylus canal: An element delivery pathway for tooth cusp biomineralization.

A detailed investigation of the stylus canal situated within the iron mineralized major lateral teeth of the chiton Acanthopleura hirtosa was undertaken in conjunction with a row-by-row examination of cusp mineralization. The canal is shown to contain columnar epithelial tissue similar to that surrounding the mineralized cusps, including the presence of iron rich particles characteristic of the iron storage protein ferritin. Within the tooth core, a previously undescribed internal pathway or plume is evident above the stylus canal, between the junction zone and mineralizing posterior face of the cusp. Plume formation coincides with the appearance of iron in the superior epithelium and the onset of mineralization at tooth row 13. The plume persists during the delivery of phosphorous and calcium into the tooth core, and is the final region of the cusp to become mineralized. The presence of the stylus canal was confirmed in a further 18 chiton species, revealing that the canal is common to polyplacophoran molluscs. These new data strongly support the growing body of evidence highlighting the importance of the junction zone for tooth mineralization in chiton teeth, and indicate that the chemical and structural environment within the tooth cusp is under far greater biological control than previously considered.