Evolution of the Sacoglossa (Mollusca, Opisthobranchia) and the ecological associations with their food plants

Evolution in the opisthobranch order Sacoglossa has been closely linked to their specialized suctorial herbivorous habits. All shelled Sacoglossa (about 20% of the species) feed on one algal genus, Caulerpa. The non-shelled Sacoglossa have 'radiated' to other diets, mainly siphonalean or septate green algae (Class Ulvophyceae). Comparing the phylogeny of sacoglossan genera with the phylogeny of the Ulvophyceae indicates that co-speciation may have taken place at the basal node of the Sacoglossa, and that host switching has taken place several times in the two non-shelled clades. It is suggested that the most important evolutionary process has been speciation by 'resource-tracking'; the resource tracked is most probably cell wall composition of the algal prey. The fossil record of extant sacoglossan genera dates back to the Eocene and, based on the fossil record of siphonalean green algae, the Sacoglossa most likely appeared in the Cretaceous. It is hypothesized that the ancestral sacoglossan was epifaunal, suctorial and herbivorous, and the 'ancestral' food plant was not Caulerpa, but filamentous, calcified, now extinct, Udoteaceae.     

Systematics and phylogeny of the Aglajidae (Opisthobranchia: Mollusca)

The generic limits within the Aglajidae are reviewed and modified, based on the study of 21 species. Navanax Pilsbry, 1895 is reinstated as a genus distinct from Aglaja. The generic placement of several species is altered from previous works. An evaluation of morphological characters suggests that each of six genera has distinctive external morphology. The systematic value of twelve characters is critically reviewed. The evolutionary relationships of the Aglajidae and its genera to other philinacean familes are discussed.     

Dietary adaptations in the teeth of murine rodents (Muridae): a test of biomechanical predictions

Functional dental theory predicts that tooth shape responds evolutionarily to the mechanical properties of food. Most studies of mammalian teeth have focused on qualitative measures of dental anatomy and have not formally tested how the functional components of teeth adapt in response to diet. Here we generated a series of predictions for tooth morphology based on biomechanical models of food processing. We used murine rodents (Old World rats and mice) to test these predictions for the relationship between diet and morphology and to identify a suite of functional dental characteristics that best predict diets. One hundred and five dental characteristics were extracted from images of the upper and lower tooth rows and incisors for 98 species. After accounting for phylogenetic relationships, we showed that species evolving plant‐dominated diets evolved deeper incisors, longer third molars, longer molar crests, blunter posteriorly angled cusps, and more expanded laterally oriented occlusal cusps than species adapting to animal‐dominated diets. Measures of incisor depth, crest length, cusp angle and sharpness, occlusal cusp orientation, and the lengths of third molars proved the best predictors of dietary adaptation. Accounting for evolutionary history in a phylogenetic discriminant function analysis notably improved the classification accuracy. Molar morphology is strongly correlated with diet and we suggest that these dental traits can be used to infer diet with good accuracy for both extinct and extant murine species.     

Sperm ultrastructure in the nudibranch genus Halgerda with reference to other Discodorididae and to Chromodorididae (Mollusca: Opisthobranchia)

Comparative sperm ultrastructure within the molluscan nudibranch genus Halgerda (Discodorididae) was examined for the first time using transmission electron microscopy (TEM), based on 17 of the 35 known species. In addition, observations on two other discodorids are made to facilitate outgroup comparison with Halgerda, including one species of Discodoris (D. boholiensis) and Asteronotus cespitosus (currently accepted as the closest sister taxon to Halgerda). Comparison was also made with some genera of the Chromodorididae in view of sperm similarities. Spermatozoa of all species examined were of the complex, helical, elongate ( approximately 300-400 micro m) type characteristic of most heterobranch gastropods. These cells exhibit the following discrete regions (in anteroposterior sequence) : an acrosomal complex (composed of a rounded, membrane-bound vesicle and a column-like pedestal); a solid, helical nucleus; an elongate, helical midpiece (composed of an axoneme and associated nine coarse fibers, an enveloping mitochondrial derivative of matrix, and paracrystalline materials and glycogen helix); an annular complex; and a short glycogen piece. Of these regions, the midpiece is by far the longest, occupying over 90% of the total sperm length. Comparison with other members of the radula-bearing cryptobranch dorids reveals several sperm similarities to other genera in the clade, particularly those of other Discodorididae and also with the Chromodorididae. Comparison with previously studied genera reveals noteworthy sperm differences within the Discodorididae. The most notable differences are the internal structure of the acrosomal pedestal (long and homogeneous in Halgerda, Discodoris; short and homogeneous in Asteronotus; long and finely striated in Rostanga; oblong with angular electron-lucent striations in Jorunna) and the internal structure of the glycogen piece. The pronounced helical keels of most Halgerda and Discodoris nuclei contrast with the weakly helical nucleus of Asteronotus. Sperm features alone do not provide a means of defining the genus Halgerda or the family Discodorididae nor do they support the monophyletic status of the caryophyllidia-bearing dorids. Important sperm characters such as the acrosome, nucleus, and midpiece can often still be determined from specimens that have been initially fixed in formalin, then stored in ethanol for extended periods of time (i.e., museum material). Of all sperm features, the mitochondrial derivative of the midpiece is the most resistant to long-term fixation : the survival of acrosomal, nuclear, and axonemal components is variable, presumably a factor of prefixation autolysis, varied primary fixation times and temperatures, formalin quality, and duration of alcohol storage.     

Scaling and adaptations of incisors and cheek teeth in caviomorph rodents (Rodentia,Hystricognathi)

The South American hystricognath rodents are one of the most diverse mammalian clades considering their occupied habitats, locomotor modes and body sizes. This might have been partly evolved by diversification of their masticatory apparatus' structure and its ecological commitment, for example, chisel‐tooth digging. In this phylogeny‐based comparative study, we test the relationship between ecological behavior and mechanical features of their incisors and molariforms. In 33 species of nine families of caviomorph rodents, we analyze incisor attributes related to structural stress resistance and molar features related with grinding capacity, for example, second moment of inertia and enamel index (EI) (enamel band length/occlusal surface area), respectively. Most of these variables scaled isometrically to body mass, with a strong phylogenetic effect. A principal component analysis discrimination on the EI clustered the species according to their geographic distribution. We presume that selective pressures in Andean–Patagonian regions, on particular feeding habits and chisel‐tooth digging behaviors, have modeled the morphological characteristics of the teeth. Subterranean/burrower ctenomyids, coruros, and plains viscachas showed the highest bending/torsion strength and anchorage values for incisors; a simplified enamel pattern in molariforms would be associated with a better grinding of the more abrasive vegetation present in more open and drier biomes. J. Morphol. 2012. © 2012 Wiley Periodicals, Inc.     

Morphological plasticity in the kelp Nereocystis luetkeana (Phaeophyceae) is sensitive to the magnitude,direction, and location of mechanical loading

Nereocystis luetkeana is a canopy-forming kelp that exhibits morphological plasticity across hydrodynamic gradients, producing broad, undulate blades in slow flow and narrow, flattened blades in fast flow, enabling thalli to reduce drag while optimizing photosynthesis. While the functional significance of this phenomenon has been well studied, the developmental and physiological mechanisms that facilitate the plasticity remain poorly understood. In this study, we conducted three experiments to characterize how the (1) magnitude, (2) direction, and (3) location of plasticity-inducing mechanical stimuli affect the morphology of Nereocystis blades. We found that applying a gradient of tensile force caused blades to grow progressively longer, narrower, less ruffled, and heavier in a linear fashion, suggesting that Nereocystis is equally well adapted for all conditions within its hydrodynamic niche. We also found that applying tension transversely across blades caused the growth response to rotate 90°, indicating that there is no substantial separation between the sites of stimulus perception and response and suggesting that a long-distance signaling mechanism, such as a hormone, is unlikely to mediate this phenomenon. Meristoderm cells showed morphological changes that paralleled those of their respective blades in this experiment, implying that tissue-level morphology is influenced by cell growth. Finally, we found that plasticity was only induced when tension was applied directly to the growing tissue, reinforcing that long-distance signaling is probably not involved and possibly indicating that the mechanism on display generally requires an intercalary meristem to facilitate mechanoperception.     

Morphological fine tuning of the feeding apparatus to proboscis length in Hesperiidae (Lepidoptera)

The form and function of the hesperiid feeding apparatus was studied in detail. The butterflies in the family Hesperiidae are of particular interest because the longest proboscis ever recorded in Papilionoidea was found in the Neotropical genus Damas. We focused on the functional morphology by comparing proboscis morphology as well as size and composition of both the stipes pump and the cibarial suction pump in skippers with short and extremely long proboscis. Results revealed that all studied Hesperiidae have the same proboscis micromorphology and sensilla endowment regardless of the proboscis length. However, the numbers of internal muscles of the proboscis, the morphology of the stipes pump as well as the pumping organs for nectar uptake are related to the proboscis length. We conclude that the low number of tip sensilla compared to proboscis length is responsible for remarkably longer manipulation times of long‐proboscid species during flower visits. The organs for proboscis movements and nectar uptake organs are well tuned to the respective proboscis length and are accordingly bigger in species with a proboscis that measures twice the body length.     

Functional phenotypic plasticity of the endolithic mytilid Leiosolenus curtus (Lischke, 1874) (Bivalvia: Mytilidae)

In Sagami Bay, Japan, Leiosolenus curtus (Lischke, 1874) bores into dead shells of rock barnacles (Tetraclita japonica) in Manazuru, calcareous sand-rock in Oiso, weathered tuff in Miura and agglomerates formed by the tubes of clam worms (Spirobranchus kraussii) in Kanaya. In order to understand the relationships between morphology and environment, the shell morphologies and genetic characteristics of L. curtus, together with the calcium content of the different bored substrata, were analysed. Individuals from Kanaya and Manazuru were characterised by a chalk-like encrustation and a more rounded and inflated shell shape, while those from Oiso and Miura had a striated encrustation. The molecular phylogenetic tree and haplotype network showed that the genetic sequences of the individuals from all investigated localities were very similar, and implied that they belong to the same species. The striated encrustation of the individuals from Oiso and Miura presumably enables them to scrape those residues not dissolved by the mucus secreted by the mantle gland, and thereby to bore into non-calcareous substrata. The more rounded and inflated shell shape of the individuals from Manazuru is thought to be advantageous for boring into thin substrata.     

The role of kleptoplasts in the survival rates of Elysia timida (Risso, 1818): (Sacoglossa: Opisthobranchia) during periods of food shortage

The importance of photosynthetic products derived from kleptoplasts in several sacoglossan species is being investigated in different fields, such as chemistry, biomolecular genetics and ecology. This study analyzes the effect of kleptoplasts on the survival rates of Elysia timida by evaluating the development of chlorophyll concentration, total length and survival rates of starved E. timida specimens kept in the light and in the dark. Although chlorophyll concentration values were similar in both cases, after 28 days specimens kept in the dark showed a greater size decrease and a lower survival rate (up to 30% lower) than those kept in the light. It is evident that kleptoplasts provide the mollusc with extra energy at the primary metabolism level to compensate for a shortage in food.     

Locomotory adaptations in entoptychine gophers (Rodentia: Geomyidae) and the mosaic evolution of fossoriality

Pocket gophers (family Geomyidae) are the dominant burrowing rodents in North America today. Their fossil record is also incredibly rich; in particular, entoptychine gophers, a diverse extinct subfamily of the Geomyidae, are known from countless teeth and jaws from Oligocene and Miocene-aged deposits of the western United States and Mexico. Their postcranial remains, however, are much rarer and little studied. Yet, they offer the opportunity to investigate the locomotion of fossil gophers, shed light on the evolution of fossoriality, and enable ecomorphological comparisons with contemporaneous rodents. We present herein a quantitative study of the cranial and postcranial remains of eight different species of entoptychine gophers as well as many contemporary rodent species. We find a range of burrowing capabilities within Entoptychinae, including semifossorial scratch-digging animals and fossorial taxa with cranial adaptations to burrowing. Our results suggest the repeated evolution of chisel-tooth digging across genera. Comparisons between entoptychine gophers and contemporaneous rodent taxa show little ecomorphological overlap and suggest that the succession of burrowing rodent taxa on the landscape may have had more to do with habitat partitioning than competition.     

Morphological plasticity and ecophysiological response of ground ivy (Glechoma hederacea,Lamiaceae) in contrasting natural habitats within its native range

Abstract

Some species intrinsically have a high invasiveness capacity, shown by high phenotypic plasticity and rapid growth, enabling a wide distribution across their native habitats and successful invasion in the introduced range. For such species, information from native habitats is critically important. An example is Glechoma hederacea, native to Eurasia but introduced and widespread in the USA. Our main objective was to investigate variation in traits of native G. hederacea populations across contrasting habitats: open, forest edge and understory. Vegetation was sampled and the ecophysiological and morphological traits were measured with accompanying environmental parameters. Results showed that in native habitats environmental conditions cover wide gradients of light and soil moisture. Plants had the highest cover in nutrient-rich, shaded habitats, representing the optimal habitat, indicating shade tolerance of G. hederacea. Plants from forest understory exhibited strong similarities in investigated traits to plants from the forest edge, even though this was a drier, sunnier habitat. Plants from open, sunny habitats experienced stress as indicated by the quantum efficiency of PSII and significantly higher sexual reproduction. Results show that G. hederacea is moderately tolerant simultaneously to shade and drought, a characteristic that has been reported for numerous invasive species, while at the same time it shares some characteristics with weedy plants.     

青藏高原高山植物的形态和解剖结构及其对环境的适应性研究进展

高山植物是一类生长于树线以上至雪线的山地植物。揭示高山植物适应环境的形态和结构特征及其内在机制,对研究全球气候变化下,植物对环境的响应和适应具有重要的理论意义。然而,国内在高山植物功能生态学的研究上相对薄弱,已有研究主要集中在对青藏高原高山植物的报道上。结合国外高山植物的相关研究报道,从形态和解剖结构两个方面对青藏高原高山植物的研究进展进行了综述,重点阐述了高山植物的形态、解剖结构及其与环境的适应性关系。植株矮小（有的呈垫状）、叶片小而厚、具有通气组织、栅栏组织多层、机械组织发达、虫媒花性状、线粒体数量多和叶绿体基粒片层少等是这一地区高山植物普遍具有的形态和结构特征。高山植物形成上述结构的特异性是高山特殊综合生态环境长期作用的结果。同时,也是高山植物对高山环境的高度适应。最后,对这一领域存在的问题以及未来研究的重点和方向进行了探讨。目的是引起国内研究者的关注,促进我国高山植物功能生态学的研究与发展。     

Sex-specific developmental plasticity of generalist and specialist predatory mites (Acari: Phytoseiidae) in response to food stress

We studied developmental plasticity under food stress in three female-biased size dimorphic predatory mite species, Phytoseiulus persimilis, Neoseiulus californicus, and Amblyseius andersoni. All three species prey on two-spotted spider mites but differ in the degree of adaptation to this prey. Phytoseiulus persimilis is a specialized spider mite predator, N. californicus is a generalist with a preference for spider mites, and A. andersoni is a broad generalist. Immature predators were offered prey patches of varying density and their survival chances, dispersal tendencies, age and size at maturity measured. Amblyseius andersoni dispersed earlier from and had lower survival chances in low density prey patches than N. californicus and P. persimilis. Age at maturity was not affected by prey density in the generalist A. andersoni, whereas both the specialist P. persimilis and the generalist N. californicus accelerated development at low prey densities. Species-specific plasticity in age at maturity reflects opposite survival strategies when confronted with limited prey: to prematurely leave and search for other food (A. andersoni) or to stay and accelerate development (P. persimilis, N. californicus). In all species, size at maturity was more plastic in females than males, indicating that males incur higher fitness costs from deviations from optimal body size.     

A model to explain spermatophore implantation in cephalopods (Mollusca: Cephalopoda) and a discussion on its evolutionary origins and significance

Male coleoid cephalopods produce spermatophores that can attach autonomously on the female's body during a complex process of evagination called the ‘spermatophoric reaction’, during which the ejaculatory apparatus and spiral filament of the spermatophore are everted and exposed to the external milieu. In some deepwater cephalopods, the reaction leads to the intradermal implantation of the spermatophore, a hitherto enigmatic phenomenon. The present study builds upon several lines of evidence to propose that spermatophore implantation is probably achieved through the combination of (1) an ‘evaginating‐tube’ mechanism performed by the everting ejaculatory apparatus and (2) the anchorage provided by the spiral filament's stellate particles. The proposed theoretical model assumes that, as it is exposed to the external milieu, each whorl of the spiral filament anchors to the surrounding tissue by means of its sharp stellate particles. As the ejaculatory apparatus tip continues evaginating, it grows in diameter and stretches lengthwise, enlarging the diameter of the whorl and propelling it, consequently tearing and pushing the anchored tissue outward and backward, and opening space for the next whorl to attach. After the ejaculatory apparatus has been everted and has perforated tissue, the cement body is extruded, possibly aiding in final attachment, and the sperm mass comes to lie inside the female tissue, encompassed by the everted ejaculatory apparatus tube. It is proposed that this unique, efficient spermatophore attachment mechanism possibly evolved in intimate relationship with the adoption of an active mode of life by coleoids. The possible roles of predation pressure and sperm competition in the evolution of this mechanism are also discussed. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 711–726.     

Movement patterns of a group of free-ranging mountain gorillas (Gorilla gorilla beringei) and their relation to food availability

Relationships between the movement patterns of free-ranging mountain gorillas (Gorilla gorilla beringei) and the abundance and distribution of foods in their home range were examined. During an 18-month field study, the ranging of one group of G. gorilla beringei was recorded on a 250 × 250 m grid system, from which measurements of frequency and duration of use, travel rate, and rate of revisitation of each quadrangle by the group were derived. Food items were sampled in selected quadrangles throughout the home range and various measures of food abundance, frequency and diversity were calculated. Analyses based on both spatial and temporal variation in food availability give supporting evidence for the prediction that mountain gorilla ranging patterns are influenced by the distribution and abundance of foods. Quality of food appears to be an important factor, as shown in analyses of yearly patterns and monthly changes in ranging. The gorillas studied spent more time in the higher quality areas of their home range, responded to a correlate of decreasing food abundance by increasing their rate of travel and area used, and revisited regions more frequently when the renewal rate of foods was clearly greater. Each of their foraging tactics can be explained as serving to increase the efficiency of harvesting foods.     

Fine-scale parallel patterns in diversity of small benthic Arctic charr (Salvelinus alpinus) in relation to the ecology of lava/groundwater habitats

It is critical to study factors that are important for origin and maintenance of biological diversity. A comparative approach involving a large number of populations is particularly useful. We use this approach to study the relationship between ecological factors and phenotypic diversity in Icelandic Arctic charr (Salvelinus alpinus). Numerous populations of small benthic charr have evolved in lava springs in Iceland. These charr appear morphologically similar, but differ in important morphological features related to feeding. We found a clear relationship between diversity in morphology, diet, and ecological factors among populations. In particular, there were clear differences in morphology and diet between fish coming from habitats where the lava spring flowed on as a stream compared to habitats where the lava spring flowed into a pond. Our study shows that ecological factors are important for the origin and maintenance of biological diversity. The relationship between phenotype and ecological factors are observed on a fine scale, when comparing numerous populations that are phenotypically similar. This strongly suggests that for understanding, managing, and conserving biological diversity important ecological variables have to be taken into the account.     

Unique features of pedicellate attachment of the upper jaw teeth in the adult gobiid fish Sicyopterus japonicus (Teleostei,Gobiidiae): Morphological and structural characteristics and development

Sicyopterus japonicus (Teleostei, Gobiidae), a hill‐stream herbivorous gobiid fish, possesses an unusual oral dentition among teleost fishes on account of its feeding habitat. By using scanning electron microscopy, light microscopy, and transmission electron microscopy, including vital staining with tetracycline, we examined the development of the attachment tissues of the upper jaw teeth in this fish. The functional teeth of S. japonicus had an asymmetrical dentine shaft. The dentine shaft attached to the underlying uniquely shaped pedicel by means of two different attachment mechanisms. At the lingual base, collagen fiber bundles connected the dentine shaft with the pedicel (hinged attachment), whereas the labial base articulated with an oval‐shaped projection of the pedicel (articulate attachment). The pedicel bases were firmly ankylosed to the crest of the thin flange of porous spongy bone on the premaxillary bone, which afforded a flange‐groove system on the labial surface of the premaxillary bone. Developmentally, the pedicel and thin flange of spongy bone were completely different mineralized attachment tissues. The pedicel had a dual origin, i.e., the dental papilla cells, which differentiated into odontoblasts that constructed the internal surface of the pedicel, and the mesenchymal cells, which differentiated into osteoblasts that formed the outer face of the pedicel. A thin flange of spongy bone was deposited on the superficial resorbed labial side of the premaxillary bone proper, and later rapid bone remodeling proceeded toward the pedicel base. These unique features of pedicellate tooth attachment for the upper jaw teeth in the adult S. japonicus are highly modified teeth for enhancing the ability of individual functional teeth to move closely over irregularities in the rock surfaces during the scraping of algae. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.