Volatile secondary metabolites as aposematic olfactory signals and defensive weapons in aquatic environments.

Olfaction is considered a distance sense; hence, aquatic olfaction is thought to be mediated only by molecules dissolved in water. Here, we challenge this view by showing that shrimp and fish can recognize the presence of hydrophobic olfactory cues by a "tactile" form of chemoreception. We found that odiferous furanosesquiterpenes protect both the Mediterranean octocoral Maasella edwardsi and its specialist predator, the nudibranch gastropod Tritonia striata, from potential predators. Food treated with the terpenes elicited avoidance responses in the cooccurring shrimp Palaemon elegans Rejection was also induced in the shrimp by the memory recall of postingestive aversive effects (vomiting), evoked by repeatedly touching the food with chemosensory mouthparts. Consistent with their emetic properties once ingested, the compounds were highly toxic to brine shrimp. Further experiments on the zebrafish showed that this vertebrate aquatic model also avoids food treated with one of the terpenes, after having experienced gastrointestinal malaise. The fish refused the food after repeatedly touching it with their mouths. The compounds studied thus act simultaneously as (i) toxins, (ii) avoidance-learning inducers, and (iii) aposematic odorant cues. Although they produce a characteristic smell when exposed to air, the compounds are detected by direct contact with the emitter in aquatic environments and are perceived at high doses that are not compatible with their transport in water. The mouthparts of both the shrimp and the fish have thus been shown to act as "aquatic noses," supporting a substantial revision of the current definition of the chemical senses based upon spatial criteria.

A consumer's guide to superorganisms.

The organism, like the molecule, the cell, and the species, is one of the fundamental levels in our hierarchical classification of life and its components. The units ranked at these levels, being concrete, particular things, are individuals in the broadest philosophical sense. But in a much narrower and more familiar sense, individual means an individual organism. Like species, the term individual is hard to define, but in most biological discourse it has meant the unit of philosophical autonomy. Some authors have attempted to revise this terminology, restricting individual to organisms, and redefining organism to include families and other units. Such semantic surgery is unnecessary if the goal is merely to justify selection at more than one level. Analogies between levels may be interesting, but many of them do not deserve to be taken seriously.

Factors promoting marine invasions: a chemoecological approach.

The Mediterranean Sea is losing its biological distinctiveness, and the same phenomenon is occurring in other seas. It gives urgency to a better understanding of the factors that affect marine biological invasions. A chemoecological approach is proposed here to define biotic conditions that promote biological invasions in terms of enemy escape and resource opportunities. Research has focused on the secondary metabolite composition of three exotic sea slugs found in Greece that have most probably entered the Mediterranean basin by Lessepsian migration, an exchange that contributes significantly to Mediterranean biodiversity. We have found toxic compounds with significant activity as feeding deterrents both in the cephalaspidean Haminoea cyanomarginata and in the nudibranch Melibe viridis. These findings led us to propose aposematism in the former and dietary autonomy in producing defensive metabolites in the latter case, as predisposing factors to the migration. In the third mollusk investigated, the anaspidean Syphonota geographica, the topic of marine invasions has been approached through a study of its feeding biology. The identification of the same compounds from both the viscera of each individual, separately analyzed, and their food, the seagrass Halophila stipulacea, implies a dietary dependency. The survival of S. geographica in the Mediterranean seems to be related to the presence of H. stipulacea. The initial invasion of this exotic pest would seem to have paved the way for the subsequent invasion of a trophic specialist that takes advantage of niche opportunities.

Magnetic resonance imaging (MRI) has failed to distinguish between smaller gut regions and larger haemal sinuses in sea urchins (Echinodermata: Echinoidea).

A response to Ziegler A, Faber C, Mueller S, Bartolomaeus T: Systematic comparison and reconstruction of sea urchin (Echinoidea) internal anatomy: a novel approach using magnetic resonance imaging. BMC Biol 2008, 6: 33.

B.F. Skinner and the Metaphysics of Darwinism.

B. F. Skinner viewed behaviorism not as the science of behavior, but a philosophy of that science. Such philosophizing is a legitimate part of a scientist's investigative behavior. He sought to eliminate confusion and error by getting rid of objectionable posits such as homunculi, vital forces, intentionalities, purposes and essences, sticking to overt behavior and spurning "mentalism." Skinner believed that there are hard analogies between learning and natural selection, such that what is appropriate in the study of one may be appropriate in the study of the other. Dispensing with teleology is but one example. Where there is selection by consequences, variation has to be taken seriously. Essentialism or typology screens out variation and leads to stereotypes. It may be viewed as treating individuals (in a broad, philosophical sense) as if they were classes. Individuals are concrete, particular things, including species and many other groups, whereas classes are abstract. Individuals can engage in processes, such as behavior. But they do not have definitions (or essences), and there are no laws of nature for them. Trying to find a definition, or an essence, for the human species is trying to find a definition for an indefinable instead of a description for a describable. Idealism has introduced a kind of mentalism into behavioral discourse that behavior analysts should scrupulously avoid. There are no laws for individuals, only for kinds of individuals, and care needs to be taken to avoid confusing laws of nature with contingent, historical fact. Skinner was a (perhaps somewhat inconsistent) realist who presupposed the uniformity of nature in his investigations. Investigative behavior may be more lawful than even he maintained.

The Suitability of Fishes as Models for Studying Appetitive Behavior in Vertebrates.

Fish have proven to be valuable models in the study of the endocrine control of appetite in response to peripheral signals of energetic and nutritional status. In parallel, a growing body of literature points to the importance of sensory experiences as factors affecting food choice in fish, with a special focus on visual and chemical signals allowing discrimination of potential foods within a 3D environment. Accordingly, waterborne compounds, such as monosaccharides or amino acids, are regarded as the main "olfactory" cues driving fish alimentary behavior. However, we recently suggested that hydrophobic molecules also allow food identification in aquatic environments and that fish actually explore a larger variety of chemosensory cues, including the olfactory/volatile compounds, when determining food palatability. In this study, we show that both homeostatic and chemosensory mechanisms involved in food intake are highly conserved in vertebrates and that the chemosensory world of fish is less different from that of terrestrial mammals than commonly thought. As a result, we support a more integrated and synthetic view of the mechanisms of chemical communication in both terrestrial and aquatic systems, which could help to ensure greater translatability of the fish models, such as the zebrafish (Danio rerio), the turquoise killifish (Nothobranchius furzeri), the goldfish (Carassius auratus), or the Japanese medaka fish (Oryzias latipes) to terrestrial vertebrates when approaching complex dynamic patterns in alimentary behavior.

The failure of morphology to contribute to the modern synthesis.

How much, if anything, morphology contributed to the modern synthesis is partly a matter of how one defines that term. In the strict sense, morphology is a purely formal discipline and had very little to contribute. Morphology may also be considered a kind of data, and when it becomes functional a better case can be made for its role in evolutionary studies. Be that as it may, the incorporation of morphology into the synthesis was a later development. The initial focus was at the populational level, including the problems of speciation, which makes sense because that was where the opportunities seemed to be. As the synthesis evolved and matured it expanded its horizons and incorporated a larger range of topics. Very little discussion of morphology occurs in the canonical writings of the so-called architects. At the time when the synthesis was supposedly complete, which was around 1950, the incorporation of morphology into it was just beginning.

Homology, convergence and parallelism.

Homology is a relation of correspondence between parts of parts of larger wholes. It is used when tracking objects of interest through space and time and in the context of explanatory historical narratives. Homologues can be traced through a genealogical nexus back to a common ancestral precursor. Homology being a transitive relation, homologues remain homologous however much they may come to differ. Analogy is a relationship of correspondence between parts of members of classes having no relationship of common ancestry. Although homology is often treated as an alternative to convergence, the latter is not a kind of correspondence: rather, it is one of a class of processes that also includes divergence and parallelism. These often give rise to misleading appearances (homoplasies). Parallelism can be particularly hard to detect, especially when not accompanied by divergences in some parts of the body.

Homology as a relation of correspondence between parts of individuals.

The recognition of correspondences has long been a fundamental activity among systematists. Advocates of Naturphilosophie, such as Lorenz Oken, drew far-fetched analogies between taxonomic groups and all sorts of other things, including the Persons of the Trinity. They treated change through time either as analogous to an ontogeny or as the product of divinely instituted laws of nature. Darwin changed things by making the taxonomic units strictly historical, implying that they are not classes but rather individuals in a broad metaphysical sense. That means that taxa are concrete, particular things, or wholes made up of parts which are themselves individuals, and that there are no laws of nature for them. Homology is a relationship of correspondence between parts of organisms that are also parts of populations and lineages. It is not a relationship of similarity, and unlike similarity it is transitive. Analogy is a relationship of correspondence between parts of organisms that are members of classes, and is not necessarily due to function. Taxa, like other individuals, can change indefinitely, and the only thing that they must share is a common ancestor. They do not share an essence, Platonic Idea or Bauplan, although "conservative characters" may be widespread in them. Iterative homology likewise is a relationship of correspondence, but the nature of that correspondence remains unclear. The difficulties of the homology concept can be overcome by treating phylogenetics and comparative biology in general as historical narrative.

The Darwinian revolution as viewed by a philosophical biologist.

Darwin proclaimed his own work revolutionary. His revolution, however, is still in progress, and the changes that are going on are reflected in the contemporary historical and philosophical literature, including that written by scientists. The changes have taken place at different levels, and have tended to occur at the more superficial ones. The new ontology that arose as a consequence of the realization that species are individuals at once provides an analytical tool for explaining what has been happening and an example of the kind of changes that seem in order. It provides a clear distinction between the roles of history and of laws of nature. Pre-Darwinian "evolution" was superficial in the sense that it treated change as either as something pre-ordained or else due to timeless laws of nature, rather than historical contingency. Darwinism puts the ontological emphasis upon concrete, particular things (individuals) and therefore delegitimizes both essentialistic and teleological ways of thinking. However, traditional ways of thinking have persisted, if not explicitly, then often as assumptions and procedures that are merely implicit or even unconscious. As a result, anti-evolutionary attitudes continue to influence the practice of evolutionary biology as well as the study of its history and philosophy.

Darwin: German mystic or French rationalist?

The notion that Charles Darwin embraced the German Romantic tradition seems plausible, given the early influence of Alexander von Humboldt. But this view fails to do justice to other scientific traditions. Darwin was a protégé of the Englishman John Stevens Henslow and was a follower of the Scott Charles Lyell. He had important debts to French scientists, notably Henri Milne-Edwards, Etienne and Isidore Geoffroy Saint-Hilaire, and Alphonse de Candolle. Many Germans were quite supportive of Darwin, but not all of these were encumbered by idealistic metaphysical baggage. Both Darwin and Anton Dohrn treated science as very much a cosmopolitan enterprise.

Sensing marine biomolecules: smell, taste, and the evolutionary transition from aquatic to terrestrial life.

The usual definition of smell and taste as distance and contact forms of chemoreception, respectively, has resulted in the belief that, during the shift from aquatic to terrestrial life, odorant receptors (ORs) were selected mainly to recognize airborne hydrophobic ligands, instead of the hydrophilic molecules involved in marine remote-sensing. This post-adaptive evolutionary scenario, however, neglects the fact that marine organisms 1) produce and detect a wide range of small hydrophobic and volatile molecules, especially terpenoids, and 2) contain genes coding for ORs that are able to bind those compounds. These apparent anomalies can be resolved by adopting an alternative, pre-adaptive scenario. Before becoming airborne on land, small molecules, almost insoluble in water, already played a key role in aquatic communication, but acting in "contact" forms of olfaction that did not require major molecular innovations to become effective at a distance in air. Rather, when air was "invaded" by volatile marine terpenoids, an expansion of the spatial range of olfaction was an incidental consequence rather than an adaptation.

Packaging and delivery of chemical weapons: a defensive trojan horse stratagem in chromodorid nudibranchs.

BACKGROUND: Storage of secondary metabolites with a putative defensive role occurs in the so-called mantle dermal formations (MDFs) that are located in the more exposed parts of the body of most and very likely all members of an entire family of marine mollusks, the chromodorid nudibranchs (Gastropoda: Opisthobranchia). Given that these structures usually lack a duct system, the mechanism for exudation of their contents remains unclear, as does their adaptive significance. One possible explanation could be that they are adapted so as to be preferentially attacked by predators. The nudibranchs might offer packages containing highly repugnant chemicals along with parts of their bodies to the predators, as a defensive variant of the strategic theme of the Trojan horse. METHODOLOGY AND PRINCIPAL FINDINGS: We detected, by quantitative (1)H-NMR, extremely high local concentrations of secondary metabolites in the MDFs of six species belonging to five chromodorid genera. The compounds were purified by chromatographic methods and subsequently evaluated for their feeding deterrent properties, obtaining dose-response curves. We found that only distasteful compounds are accumulated in the reservoirs at concentrations that far exceed the values corresponding to maximum deterrent activity in the feeding assays. Other basic evidence, both field and experimental, has been acquired to elucidate the kind of damage that the predators can produce on both the nudibranchs' mantles and the MDFs. SIGNIFICANCE: As a result of a long evolutionary process that has progressively led to the accumulation of defensive chemical weapons in localized anatomical structures, the extant chromodorid nudibranchs remain in place when molested, retracting respiratory and chemosensory organs, but offering readily accessible parts of their body to predators. When these parts are masticated or wounded by predators, breakage of the MDFs results in the release of distasteful compounds at extremely high concentration in a way that maximizes their repugnant impact.

Coloration and defense in the nudibranch gastropod Hypselodoris fontandraui.

The striking color patterns of chromodorid (and other) nudibranchs appear to be indicative of aposematism. In Müllerian mimicry, all the mimic species have a defense mechanism. It has been proposed that a group of blue, white, and yellow Mediterranean and northeastern Atlantic species of the genus Hypselodoris form a Müllerian mimetic circle. One of these, H. fontandraui, lacks the mantle dermal formations (repugnatorial glands) that are typically found in other members of this circle and are reservoirs of feeding deterrent compounds. It therefore seemed possible that this animal lacks chemical defense and acts like a Batesian mimic. Within this study, we found that this nudibranch contains the furanosesquiterpenoid tavacpallescensin, most probably derived from sponges of the genus Dysidea, upon which it probably feeds. The metabolite concentrations were measured from samples of the mantle rim, other external parts, and internal organs. Concentrations were about 4 times higher in the mantle rim than in the other external parts, and more than 20 times higher in the mantle rim than in the internal organs, considerably exceeding the threshold value of concentration showing the maximum dose effect as feeding deterrent against the crustacean Palaemon elegans. In conclusion, the reported data clearly demonstrate that H. fontandraui is chemically defended in much the same way as its aposematic, co-occurring, and blue-colored congeners within the Müllerian mimetic circle and is not a Batesian mimic.

Anton Dohrn and the problems of 19th century phylogenetic morphology.

According to Anton Dohrn, evolutionary development was performed in a single progressive lineage where some proto-annelid initiated an evolutionary development that went straight on via annelids and lower vertebrates to man. From that line, a kind of metamorphosing nature, certain branches were derived, like protists or worms or even tunicates, which Dohrn thought off as degenerating groups. With that concept Dohrn came close to typological ideas of his time. Nevertheless, recent evo-devo literature seems to be influenced by Dohrn's outline of evolution.

Evolution and development: past, present, and future.

The paper tries to set right certain ideas about the history of evolutionary developmental biology. The main point is, that we had to enface the dominance of a comparative approach towards evolutionary developmental biology before 1900, which even later on was effective in Russia, for example, till the 1930s. The problem of the experimentalist approach set against this tradition was and is that there is no concept of gestalt that may allow to integrate the former comparative views and the modern mechanistic interpretations. We argue, that it would be wrong just to describe the comparative tradition as being outdated, as it may allow to get the framework for a dynamical concept of Gestalt that may integrate the ideas of morphogenesis and pattern formation worked out in evo-devo recently.

Sexual selection in hermaphrodites: where did our ideas come from?

Interpretations of hermaphroditism have been influenced by the old idea that organisms can be arranged in a series from lower to higher, with human beings at the top, leading toward the angels and God (the scala naturae). The consequent notion that hermaphroditism is a primitive condition is still with us. Such issues need to be addressed empirically, in a phylogenetic context. Darwin's theory of sexual selection provided the key to understanding sex switches, but it was not invoked until 1969 when it was conjoined with ideas about relative size influenced by the work of Bernhard Rensch. In principle the problem could have been solved a century earlier, and genetics was misleading rather than helpful. What really helped was an appreciation of Darwin's nonteleological way of thinking.

PERSPECTIVE: DARWIN, PROGRESS, AND ECONOMIC PRINCIPLES.

Darwin's concept of progress was an economic one, with the accumulation of adaptations having a strong analogy to technological innovations. This interpretation makes it easier to understand his differences with Lamarck and others whose views he considered metaphysically objectionable. It also clarifies his relationship to Malthus and such features of his theory as the episodic nature of evolutionary change. His position is consistent with modern theories of biotic invasions and long-term evolutionary trends. It also accords well with current efforts to produce a synthesis between biology and economics.