Dollo's law and the re-evolution of shell coiling

Gastropods have lost the quintessential snail feature, the coiled shell, numerous times in evolution. In many cases these animals have developed a limpet morphology with a cap-shaped shell and a large foot. Limpets thrive in marginal habitats such as hydrothermal vents, the high-energy rocky intertidal areas and fresh water, but they are considered to be evolutionary dead-ends, unable to re-evolve a coiled shell and therefore unable to give rise to the diversity seen among coiled snails. The re-evolution of a coiled shell, or any complex character, is considered unlikely or impossible (Dollo's law) because the loss of the character is followed by the loss of the genetic architecture and developmental mechanisms that underlie that character. Here, we quantify the level of coiling in calyptraeids, a family of mostly uncoiled limpets, and show that coiled shells have re-evolved at least once within this family. These results are the first demonstration, to our knowledge, of the re-evolution of coiling in a gastropod, and show that the developmental features underlying coiling have not been lost during 20-100 Myr of uncoiled evolutionary history. This is the first example of the re-evolution of a complex character via a change in developmental timing (heterochrony) rather than a change in location of gene expression (heterotopy).     

Mathematical determination of coiled shell volumes and surface areas

Mathematical models of shells enable researchers to estimate the maximum possible sizes of organisms that once occupied fossil shells. In this study, a whorl-by-whorl method of determining coiled shell volumes and surface areas is introduced. The whorl-by-whorl analysis yielded results that were more accurate than those obtained from a model that assumes isometric growth, when both were used to calculate volumes of gastropod shells. The whorl-by-whorl method is more laborious, but it is better suited for the analysis of shells exhibiting allometric variation than are methods that use models of isometric growth.     

Genetic Basis of a Violation of Dollo’s Law: Re-Evolution of Rotating Sex Combs in Drosophila bipectinata

Phylogenetic analyses suggest that violations of “Dollo’s law”—that is, re-evolution of lost complex structures—do occur, albeit infrequently. However, the genetic basis of such reversals has not been examined. Here, we address this question using the Drosophila sex comb, a recently evolved, male-specific morphological structure composed of modified bristles. In some species, sex comb development involves only the modification of individual bristles, while other species have more complex “rotated” sex combs that are shaped by coordinated migration of epithelial tissues. Rotated sex combs were lost in the ananassae species subgroup and subsequently re-evolved, ∼12 million years later, in Drosophila bipectinata and its sibling species. We examine the genetic basis of the differences in sex comb morphology between D. bipectinata and D. malerkotliana, a closely related species with a much simpler sex comb representing the ancestral condition. QTL mapping reveals that >50% of this difference is controlled by one chromosomal inversion that covers ∼5% of the genome. Several other, larger inversions do not contribute appreciably to the phenotype. This genetic architecture suggests that rotating sex combs may have re-evolved through changes in relatively few genes. We discuss potential developmental mechanisms that may allow lost complex structures to be regained.     

Evolution: have wings come,gone and come again?

Can complex traits be re-evolved by lineages that have lost them? Phylogenetic study now suggests that wings may indeed have reappeared several times within the ancestrally wingless stick insects.     

Phylogenetic evidence for colour pattern convergence in toxic pitohuis: Müllerian mimicry in birds?

Bird species in the genus Pitohui are chemically defended by a potent neurotoxic alkaloid in their skin and feathers. The two most toxic pitohui species, the hooded pitohui (Pitohui dichrous) and the variable pitohui (Pitohui kirhocephalus), are sometimes strikingly patterned and, in certain portions of their geographical ranges, both species share a nearly identical colour pattern, whereas in other areas they do not. Müllerian mimicry (the mutual resemblance of two chemically defended prey species) is common in some other animal groups and Pitohui birds have been suggested as one of the most likely cases in birds. Here, we examine pitohui plumage evolution in the context of a well-supported molecular phylogeny and use a maximum likelihood approach to test for convergent evolution in coloration. We show that the 'mimetic' phenotype is ancestral to both species and that the resemblance in most races is better explained by a shared ancestry. One large clade of P. kirhocephalus lost this mimetic phenotype early in their evolution and one race nested deep within this clade appears to have re-evolved this phenotype. These latter findings are consistent with the hypothesis that Müllerian mimicry is driving the evolution for a similar colour pattern between P. dichrous, but only in this one clade of P. kirhocephalus     

The structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state

Molecular chaperones assist protein folding by facilitating their "forward" folding and preventing aggregation. However, once aggregates have formed, these chaperones cannot facilitate protein disaggregation. Bacterial ClpB and its eukaryotic homolog Hsp104 are essential proteins of the heat-shock response, which have the remarkable capacity to rescue stress-damaged proteins from an aggregated state. We have determined the structure of Thermus thermophilus ClpB (TClpB) using a combination of X-ray crystallography and cryo-electron microscopy (cryo-EM). Our single-particle reconstruction shows that TClpB forms a two-tiered hexameric ring. The ClpB/Hsp104-linker consists of an 85 A long and mobile coiled coil that is located on the outside of the hexamer. Our mutagenesis and biochemical data show that both the relative position and motion of this coiled coil are critical for chaperone function. Taken together, we propose a mechanism by which an ATP-driven conformational change is coupled to a large coiled-coil motion, which is indispensable for protein disaggregation.     

The Paleozoic evolution of the gastropod larval shell: larval armor and tight coiling as a result of predation‐driven heterochronic character displacement

Early and middle Paleozoic gastropod protoconchs generally differ strongly from their corresponding adult morphologies, that is, most known protoconchs are smooth and openly coiled, whereas the majority of adult shells are ornamented and tightly coiled. In contrast, larval and adult shells of late Paleozoic gastropods with planktotrophic larval development (Caenogastropoda, Neritimorpha) commonly resemble each other in shape and principle ornamentation. This is surprising because habitat and mode of life of planktonic larvae and benthic adults differ strongly from each other. Generally, late Paleozoic to Recent protoconchs are tightly coiled. This modern type of larval shell resembles the adult shell morphology and was obviously predisplaced onto the larval stage during the middle Paleozoic. The oldest known planktonic‐armored (strongly ornamented) larval shells are known from the late Paleozoic. However, smooth larval shells are also common among the studied late Paleozoic gastropods. The appearance of larval armor at the beginning of the late Paleozoic could reflect an increase of predation pressure in the plankton. Although there are counter examples in which larval and adult shell morphology differ strongly from each other, there is statistical evidence for a heterochronic predisplacement of adult characters onto the larval stage. Larval and adult shells are built in the same way, by accretionary secretion at the mantle edge. It is likely that the same underlying gene expression is responsible for that. If so, similarities of larval and adult shell may be explained by gene sharing, whereas differences may be due to different (planktic vs. benthic life) epigenetic patterns.     

The prosicular stage of Rhabdopleura (Pterobranchia: Hemichordata)

After settling, the larva of Rhabdopleura surrounds itself with a collagenous dome. Later, the zooid breaks through the wall of the dome and builds the horizontal tube part of the coenecium on to the dome.
The dome is a layered structure, unknown in other parts of the coenecium. whereas the horizontal tube is made up of rings in the classical manner of the adult coenecium. The construction of these two parts is different. The techniques used to reinforce the horizontal tube show a marked similarity to the cortical bandages recently described in the fossil graptolites, and give support to the claim that they are ancestral to Rhabdopleura. There are two sorts of early horizontal tube, one is a straight tube, and the other is longer and coiled. The hole in the dome through which the zooid emerges to build the horizontal tube is probably produced by a chemical boring of the zooid, and supports the hypothesis that the zooids can bore holes in shells and corals.     

The phylogeny of the Pentaschistis clade (Danthonioideae, Poaceae) based on chloroplast DNA, and the evolution and loss of complex characters

We construct a species-level phylogeny for the Pentaschistis clade based on chloroplast DNA, from the following regions: trnL-F, trnT-L, atpB-rbcL, rpL16, and trnD-psbA. The clade comprises 82 species in three genera, Pentaschistis, Pentameris, and Prionanthium. We demonstrate that Prionanthium is nested in Pentaschistis and that this clade is sister to a clade of Pentameris plus Pentaschistis tysonii. Forty-three of the species in the Pentaschistis clade have multicellular glands and we use ancestral character state reconstruction to show that they have been gained twice or possibly once, and lost several times. We suggest that the maintenance, absence, loss, and gain of glands are correlated with leaf anatomy type, and additionally that there is a difference in the degree of diversification of lineages that have these different character combinations. We propose that both glands and sclerophyllous leaves act as defense systems against herbivory, and build a cost/benefit model in which multicellular glands or sclerophyllous leaves are lost when the alternative defense system evolves. We also investigate the association between leaf anatomy type and soil nutrient type on which species grow. There is little phylogenetic constraint in soil nutrient type on members of the Pentaschistis clade, with numerous transitions between oligotrophic and eutrophic soils. However, only orthophyllous-leaved species diversify on eutrophic soils. We suggest that the presence of these glands enables the persistence of orthophyllous lineages and therefore diversification of the Pentaschistis clade on eutrophic as well as oligotrophic soils.     

Evolution of male morphology in the ant genus Cardiocondyla

The ant genus Cardiocondyla is characterized by a striking male polymorphism, with wingless, local fighter males (ergatoid males) with life-long spermatogenesis, and winged, peaceful disperser males with limited sperm supply. We examined the evolution of male morphology by reconstructing the phylogeny of Cardiocondyla from sequences of the mitochondrial COI/COII and 16S RNA genes from 13 of the 15 species, of which males are known. Data suggest that male polymorphism is ancestral and that winged males were lost convergently in several taxa, such as C. elegans, C. batesii, and C. mauritanica. Saber-shaped mandibles and lethal fighting among adult ergatoid males might probably have been the original condition, from which strong, shear-shaped mandibles and attacks directed predominantly against freshly eclosed, not yet sclerotized males might have evolved once. The evolution of queen number from ancestral polygyny to derived monogyny appears to be associated with a switch in the behavior of ergatoid males from fighting to mutual tolerance.     

Preferential predatory peeling: Ammonoid vs. nautiloid shells from the Upper Carboniferous of Texas,USA

Narrow groove-like excavations on ammonoid and coiled nautiloid shells are rare in Upper Carboniferous units from Texas, USA. The morphological characteristics of the excavation grooves typically are confined to the ventral and ventrolateral parts of the outer whorl of the shell, are narrower than the length, and have irregular edges where small segments or chips of shells have been removed. Analysis of these features reveals a statistically significant preferential occurrence on ammonoids (1.195% of ca. 3515 specimens) as compared to coiled nautiloids (0.506% of ca. 2965 specimens). The ammonoids typically have longer excavations that penetrate the phragmocone more frequently than those observed in the coiled nautiloids. The groove-like excavations were probably formed by the removal and peeling of shell material by one or more predatory or scavenging arthropods to obtain organic material (tissue and membranes) within the ammonoid and nautiloid body chambers and phragmocones. The excavations probably occurred when the cephalopod was alive (i.e., the cause of death) or shortly after the cephalopod's death. There is no evidence that the excavations are related to sheltering by the excavating organism.     

ADAPTATION FROM RESTRICTED GEOMETRIES: THE SHELL INCLINATION OF TERRESTRIAL GASTROPODS

The adaptations that occur for support and protection can be studied with regard to the optimal structure that balances these objectives with any imposed constraints. The shell inclination of terrestrial gastropods is an appropriate model to address this problem. In this study, we examined how gastropods improve shell angles to well‐balanced ones from geometrically constrained shapes. Our geometric analysis and physical analysis showed that constantly coiled shells are constrained from adopting a well‐balanced angle; the shell angle of such basic shells tends to increase as the spire index (shell height/width) increases, although the optimum angle for stability is 90° for flat shells and 0° for tall shells. Furthermore, we estimated the influences of the geometric rule and the functional demands on actual shells by measuring the shell angles of both resting and active snails. We found that terrestrial gastropods have shell angles that are suited for balance. The growth lines of the shells indicated that this adaptation depends on the deflection of the last whorl: the apertures of flat shells are deflected downward, whereas those of tall shells are deflected upward. Our observations of active snails demonstrated that the animals hold their shells at better balanced angles than inactive snails.     

The evolution of milk secretion and its ancient origins

Lactation represents an important element of the life history strategies of all mammals, whether monotreme, marsupial, or eutherian. Milk originated as a glandular skin secretion in synapsids (the lineage ancestral to mammals), perhaps as early as the Pennsylvanian period, that is, approximately 310 million years ago (mya). Early synapsids laid eggs with parchment-like shells intolerant of desiccation and apparently dependent on glandular skin secretions for moisture. Mammary glands probably evolved from apocrine-like glands that combined multiple modes of secretion and developed in association with hair follicles. Comparative analyses of the evolutionary origin of milk constituents support a scenario in which these secretions evolved into a nutrient-rich milk long before mammals arose. A variety of antimicrobial and secretory constituents were co-opted into novel roles related to nutrition of the young. Secretory calcium-binding phosphoproteins may originally have had a role in calcium delivery to eggs; however, by evolving into large, complex casein micelles, they took on an important role in transport of amino acids, calcium and phosphorus. Several proteins involved in immunity, including an ancestral butyrophilin and xanthine oxidoreductase, were incorporated into a novel membrane-bound lipid droplet (the milk fat globule) that became a primary mode of energy transfer. An ancestral c-lysozyme lost its lytic functions in favor of a role as α-lactalbumin, which modifies a galactosyltransferase to recognize glucose as an acceptor, leading to the synthesis of novel milk sugars, of which free oligosaccharides may have predated free lactose. An ancestral lipocalin and an ancestral whey acidic protein four-disulphide core protein apparently lost their original transport and antimicrobial functions when they became the whey proteins β-lactoglobulin and whey acidic protein, which with α-lactalbumin provide limiting sulfur amino acids to the young. By the late Triassic period (ca 210 mya), mammaliaforms (mammalian ancestors) were endothermic (requiring fluid to replace incubatory water losses of eggs), very small in size (making large eggs impossible), and had rapid growth and limited tooth replacement (indicating delayed onset of feeding and reliance on milk). Thus, milk had already supplanted egg yolk as the primary nutrient source, and by the Jurassic period (ca 170 mya) vitellogenin genes were being lost. All primary milk constituents evolved before the appearance of mammals, and some constituents may have origins that predate the split of the synapsids from sauropsids (the lineage leading to 'reptiles' and birds). Thus, the modern dairy industry is built upon a very old foundation, the cornerstones of which were laid even before dinosaurs ruled the earth in the Jurassic and Cretaceous periods.     

Larval and juvenile gastropods from a Carboniferous black shale: palaeoecology and implications for the evolution of the Gastropoda

A horizon in the late Visean Ruddle Shale from Arkansas contains the oldest well-preserved gastropod protoconchs known from the Americas. The gastropod fauna consists of a diverse larval shell assemblage and a low diversity assemblage of juvenile gastropods that probably had a benthic life habit. Gastropod larval shells are always isolated, i.e. the gastropods did not complete their life cycle (no metamorphosis) and were unable to become benthic. This was caused by unfavorable environmental conditions on the soft muddy bottom that was probably due to anaerobic to exaerobic conditions. The absence or scarcity of bioturbation caused by invertebrate detritus or sediment feeders in both shale and concretions (formed before compaction) favored preservation of the delicate larval shells. The lack or scarcity of infauna and bioturbation as well as the low diversity of the presumed benthos supports an interpretation of a quasi-anaerobic to exaerobic benthic environment. The superbly preserved larval shells demonstrate that there are more caenogastropod clades present in the late Palaeozoic than suggested previously. Some larval shell types have an openly coiled first whorl followed by a planktotrophic larval shell; openly coiled initial whorls are unknown from modern caenogastropods. The vetigastropods have a smooth protoconch of two whorls clearly demarked from the following whorls - a pattern unknown in modern vetigastropods which have a protoconch of less than one whorl and build no larval shell during their planktonic stage. This could indicate a link between Palaeozoic vetigastropods and the caenogastropods.     

Evolution of perianth and stamen characteristics with respect to floral symmetry in Ranunculales

BACKGROUND AND AIMS: Floral symmetry presents two main states in angiosperms, namely polysymmetry and monosymmetry. Monosymmetry is thought to have evolved several times independently from polysymmetry, possibly in co-adaptation with specialized pollinators. Monosymmetry commonly refers to the perianth, even though associated androecium modifications have been reported. The evolution of perianth symmetry is examined with respect to traits of flower architecture in the Ranunculales, the sister group to all other eudicots, which present a large diversity of floral forms. METHODS: Characters considered were perianth merism, calyx, corolla and androecium symmetry, number of stamens and spurs. Character evolution was optimized on a composite phylogenetic tree of Ranunculales using maximum parsimony. KEY RESULTS: The ancestral state for merism could not be inferred because the basalmost Eupteleaceae lack a perianth and have a variable number of stamens. The Papaveraceae are dimerous, and the five other families share a common trimerous ancestor. Shifts from trimery to dimery (or reverse) are observed. Pentamery evolved in Ranunculaceae. Ranunculales except Eupteleaceae, present a polysymmetric ancestral state. Monosymmetry evolved once within Papaveraceae, Ranunculaceae and Menispermaceae (female flowers only). Oligandry is the ancestral state for all Ranunculales, and polyandry evolved several times independently, in Papaveraceae, Menispermaceae, Berberidaceae and Ranunculaceae, with two reversions to oligandry in the latter. The ancestral state for androecium symmetry is ambiguous for the Ranunculales, while polysymmetry evolved immediately after the divergence of Eupteleaceae. A disymmetric androecium evolved in Papaveraceae. The ancestral state for spurs is none. Multiple spurs evolved in Papaveraceae, Berberidaceae and Ranunculaceae, and single spurs occur in Papaveraceae and Ranunculaceae. CONCLUSIONS: The evolution of symmetry appears disconnected from changes in merism and stamen number, although monosymmetry never evolved in the context of an open ground plan. In bisexual species, monosymmetry evolved coincidently with single spurs, allowing us to propose an evolutionary scenario for Papaveraceae.     

PHYLOGENY OF THE TRIBE CERATAPHIDINI (HOMOPTERA) AND THE EVOLUTION OF THE HORNED SOLDIER APHIDS

The horned soldier aphids of the Cerataphidini, unlike most social insects that reside in nests, live on the open surface of plants. The lack of a nest and other obvious ecological correlates makes it unclear why secondary-host soldiers might have evolved. Here I present a molecular phylogenetic analysis of 32 species of the Cerataphidini, including 10 species from the genera Ceratovacuna and Pseudoregma that produce horned soldiers. The phylogeny suggests that horned soldiers evolved once and were lost once or twice. Most horned soldiers are a morphologically specialized caste and two species that have unspecialized soldiers are independently derived from species with specialized castes. The genus Ceratovacuna appears to have undergone a relatively rapid radiation. Mapping secondary-host plants and geographic ranges onto the phylogeny suggests that bamboos were the ancestral secondary-host plants and that the Asian tropics and subtropics were the ancestral geographic regions for the genera Astegopteryx, Ceratoglyphina, Ceratovacuna Chaitoregma, and Pseudoregma and possibly for the entire tribe. There is evidence for vicariant events that separate the tropical and subtropical lineages in all of the major lineages of the tribe and for dispersal of some lineages. Based on these results, I present hypotheses for the causes and consequences of horned-soldier evolution.     

‘Viable but non-culturable cells’ are dead

Most bacteria lead lives of quiet desperation, so they sleep. By sleeping, bacteria survive ubiquitous stress, such as antibiotics, and can resuscitate to reconstitute infections. As for other nearly universal and highly regulated processes such as biofilm formation, in persistence, a small population of cells have an elegantly-regulated pathway to become dormant. By inactivating their ribosomes, persister cells sleep through stress and resuscitate once (i) the stress is removed, (ii) nutrients are presented and (iii) ribosome content reaches a threshold. During stress, cells often become spheroid and die, becoming hollow, membrane-enclosed vessels. How cellular content is lost is unclear, but it is obvious that these ‘cell shells’ are dead; i.e., ‘There's no there there’. Critically, due to their intact membranes, the shells appear with membrane-impenetrant stains as ‘viable’ particles. Unfortunately, the microbiology field of ‘viable but non-culturable cells’ (VBNCs), though important for demonstrating the existence of dormant bacteria as a result of myriad stress states, has often mistaken these non-viable shells as viable particles that mysteriously may be reborn, when an appropriate incantation is made. We argue here, based on experimental data, that if resuscitation occurs, it is the persister (always-viable) cell population that revives, rather than the cell husks, which are dead.     

Complicated evolution of the caprellid (Crustacea: Malacostraca: Peracarida: Amphipoda) body plan,reacquisition or multiple losses of the thoracic limbs and pleons

The Caprellidea (Crustacea) have undergone an interesting morphological evolution from their ancestral gammarid-like form. Although most caprellid families have markedly reduced third and fourth pereopods (the walking thoracic limbs) and pleons (the posterior body parts), one family, Caprogammaridae, has developed pleon with swimming appendages (pleopods), whereas another family, Phtisicidae, possesses well-developed functional third and fourth pereopods. The unique character status of these families implies that there has been reacquisition or multiple losses of both pereopods and the pleon within the Caprellidea lineages. Although the Caprellidea are fascinating animals for the study of morphological evolution, the phylogenetic relationships among the Caprellidea are poorly understood. One obstacle to studying the evolution of the Caprellidea is the difficulty of collecting samples of caprogammarid species. In this study, we obtained live samples of a Caprogammaridae species and confirmed that its pleon and pleopods could perform similar locomotive functions and swimming movements as observed in gammarids. From the phylogenetic analyses on 18S ribosomal RNA gene sequences, we identified three distinct clades of Caprellidea. The ancestral state reconstruction based on the obtained phylogeny suggested that once lost, the third and fourth pereopods were regained in the Phtisicidae, while the pleon was regained in the Caprogammaridae, while we could not exclude the possibility of independent losses. In either case, the caprellid lineage underwent a quite complicated morphological evolution, and possibly the Caprellidea may be an exception to Dollo’s law.     

The Evolution and Structure Prediction of Coiled Coils across All Genomes

Coiled coils are α-helical interactions found in many natural proteins. Various sequence-based coiled-coil predictors are available, but key issues remain: oligomeric state and protein-protein interface prediction and extension to all genomes. We present SpiriCoil (http://supfam.org/SUPERFAMILY/spiricoil), which is based on a novel approach to the coiled-coil prediction problem for coiled coils that fall into known superfamilies: hundreds of hidden Markov models representing coiled-coil-containing domain families. Using whole domains gives the advantage that sequences flanking the coiled coils help. SpiriCoil performs at least as well as existing methods at detecting coiled coils and significantly advances the state of the art for oligomer state prediction. SpiriCoil has been run on over 16 million sequences, including all completely sequenced genomes (more than 1200), and a resulting Web interface supplies data downloads, alignments, scores, oligomeric state classifications, three-dimensional homology models and visualisation. This has allowed, for the first time, a genomewide analysis of coiled-coil evolution. We found that coiled coils have arisen independently de novo well over a hundred times, and these are observed in 16 different oligomeric states. Coiled coils in almost all oligomeric states were present in the last universal common ancestor of life. The vast majority of occasions that individual coiled coils have arisen de novo were before the last universal common ancestor of life; we do, however, observe scattered instances throughout subsequent evolutionary history, mostly in the formation of the eukaryote superkingdom. Coiled coils do not change their oligomeric state over evolution and did not evolve from the rearrangement of existing helices in proteins; coiled coils were forged in unison with the fold of the whole protein.