Behavioural flexibility and problem-solving in a tropical lizard

The role of behavioural flexibility in responding to new or changing environmental challenges is a central theme in cognitive ecology. Studies of behavioural flexibility have focused mostly on mammals and birds because theory predicts that behavioural flexibility is favoured in species or clades that exploit a diversity of habitats or food sources and/or have complex social structure, attributes not associated with ectothermic vertebrates. Here, we present the results of a series of experiments designed to test cognitive abilities across multiple cognitive modules in a tropical arboreal lizard: Anolis evermanni. This lizard shows behavioural flexibility across multiple cognitive tasks, including solving a novel motor task using multiple strategies and reversal learning, as well as rapid associative learning. This flexibility was unexpected because lizards are commonly believed to have limited cognitive abilities and highly stereotyped behaviour. Our findings indicate that the cognitive abilities of A. evermanni are comparable with those of some endothermic species that are recognized to be highly flexible, and strongly suggest a re-thinking of our understanding of the cognitive abilities of ectothermic tetrapods and of the factors favouring the evolution of behavioural flexibility.     

Motion perception and visual signal design in Anolis lizards

Anolis lizards communicate with displays consisting of motion of the head and body. Early portions of long-distance displays require movements that are effective at eliciting the attention of potential receivers. We studied signal-motion efficacy using a two-dimensional visual-motion detection (2DMD) model consisting of a grid of correlation-type elementary motion detectors. This 2DMD model has been shown to accurately predict Anolis lizard behavioural response. We tested different patterns of artificially generated motion and found that an abrupt 0.3° shift of position in less than 100 ms is optimal. We quantified motion in displays of 25 individuals from five species. Four species employ near-optimal movement patterns. We tested displays of these species using the 2DMD model on scenes with and without moderate wind. Display movements can easily be detected, even in the presence of windblown vegetation. The fifth species does not typically use the most effective display movements and display movements cannot be discerned by the 2DMD model in the presence of windblown vegetation. A number of Anolis species use abrupt up-and-down head movements approximately 10 mm in amplitude in displays, and these movements appear to be extremely effective for stimulating the receiver visual system.     

Convergent exaptation and adaptation in solitary island lizards

Independent evolutionary lineages often display similar characteristics in comparable environments. Three kinds of historical hypotheses could explain this convergence. The first is adaptive and evolutionary: nonrandom patterns may result from analogous evolutionary responses to shared conditions. The second explanation is exaptive and ecological: species may be filtered by their suitability for a particular type of environment. The third potential explanation is a null hypothesis of random colonization from a historically nonrandom source pool. Here we demonstrate that both exaptation and adaptation have produced convergent similarity in different size-related characters of solitary island lizards. Large sexual size dimorphism results from adaptive response to solitary existence; uniform, intermediate size results from ecological filtering of potential colonizers. These results demonstrate the existence of deterministic exaptive convergence and suggest that convergent phenomena may require historical explanations that are ecological as well as evolutionary.     

Body size evolution simultaneously creates and collapses species boundaries in a clade of scincid lizards

Speciation is generally viewed as an irreversible process, although habitat alterations can erase reproductive barriers if divergence between ecologically differentiated species is recent. Reversed speciation might also occur if geographical contact is established between species that have evolved the same reproductive isolating barrier in parallel. Here, we demonstrate a loss of intrinsic reproductive isolation in a clade of scincid lizards as a result of parallel body size evolution, which has allowed for gene flow where large-bodied lineages are in secondary contact. An mtDNA phylogeny confirms the monophyly of the Plestiodon skiltonianus species complex, but rejects that of two size-differentiated ecomorphs. Mate compatibility experiments show that the high degree of body size divergence imposes a strong reproductive barrier between the two morphs; however, the strength of the barrier is greatly diminished between parallel-evolved forms. Since two large-bodied lineages are in geographical contact in the Sierra Nevada Mountains of California, we were also able to test for postzygotic isolation under natural conditions. Analyses of amplified fragment length polymorphisms show that extensive gene exchange is occurring across the contact zone, resulting in an overall pattern consistent with isolation by distance. These results provide evidence of reversed speciation between clades that diverged from a common ancestor more than 12Myr ago.     

Enzyme function and polymorphism: A test in two Anolis lizard species

Electrophoretic surveys of two lizard species were used to test hypotheses that relate levels of enzyme variability to enzyme function (single-substrate versus multiple-substrate enzymes, regulatory versus nonregulatory enzymes). Anolis roquet behaviorally regulates its body temperature, but its congener A. gundlachi is passive to variations in the thermal environment. As a result, populations of A. gundlachi probably experience the thermal environment as temporally coarse-grained, whereas populations of A. roquet do not. We therefore predicted that A. gundlachi would exhibit greater enzyme heterozygosity than A. roquet and that different enzyme classes would contribute disproportionately to this interspecific difference. The data show (1) that A. gundlachi does have a higher heterozygosity and (2) that this difference appears to result from high levels of heterozygosity at loci coding for multiple-substrate enzymes. The dichotomy between regulatory and nonregulatory enzymes offers no explanation for the variability in heterozygosity among enzyme loci in these species.E.Z. was supported by a grant from the Natural Sciences and Engineering Council of Canada. The study was accomplished while P.E.H. held a postdoctoral fellowship from the Killam Trust of Dalhousie University and a grant from the Research Development Fund of Dalhousie University. The collection of material was made possible by grants (to P.E.H.) from National Science Foundation (DEB 75-16334), the Explorers Club of New York, Sigma Xi, and the Richmond and Anderson Funds of Harvard University. We thank Dr. D. W. Foltz for his help with the calculations.     

Cryptic diversity in vertebrates: molecular data double estimates of species diversity in a radiation of Australian lizards (Diplodactylus,Gekkota)

A major problem for biodiversity conservation and management is that a significant portion of species diversity remains undocumented (the ‘taxonomic impediment’). This problem is widely acknowledged to be dire among invertebrates and in developing countries; here, we demonstrate that it can be acute even in conspicuous animals (reptiles) and in developed nations (Australia). A survey of mtDNA, allozyme and chromosomal variation in the Australian gecko, genus Diplodactylus, increases overall species diversity estimates from 13 to 29. Four nominal species each actually represent multi-species complexes; three of these species complexes are not even monophyletic. The high proportion of cryptic species discovered emphasizes the importance of continuing detailed assessments of species diversity, even in apparently well-known taxa from industrialized countries.     

A new species of Alopoglossus lizard (Squamata,Gymnophthalmidae) from the tropical Andes,with a molecular phylogeny of the genus

We describe a new species of Alopoglossus from the Pacific slopes of the Andes in northern Ecuador based on morphological and molecular evidence. The new species differs most significantly from all other congeners in having a double longitudinal row of widened gular scales, lanceolate dorsal scales in transverse rows, 29–32 dorsal scales in a transverse row at midbody, and 4 longitudinal rows of ventrals at midbody. It is most similar in morphology to A. festae, the only species of Alopoglossus currently recognized in western Ecuador. We analyze the phylogenetic relationships among species of Alopoglossus based on the mitochondrial gene ND4. Cis-Andean [east of the Andes] and Trans-Andean [west of the Andes] species are nested in two separate clades, suggesting that the uplift of these mountains had an important effect in the diversification of Alopoglossus. In addition, we present an updated key to the species of Alopoglossus.     

Nitrification expanded: discovery,physiology and genomics of a nitrite-oxidizing bacterium from the phylum Chloroflexi

Nitrite-oxidizing bacteria (NOB) catalyze the second step of nitrification, a major process of the biogeochemical nitrogen cycle, but the recognized diversity of this guild is surprisingly low and only two bacterial phyla contain known NOB. Here, we report on the discovery of a chemolithoautotrophic nitrite oxidizer that belongs to the widespread phylum Chloroflexi not previously known to contain any nitrifying organism. This organism, named Nitrolancetus hollandicus, was isolated from a nitrifying reactor. Its tolerance to a broad temperature range (25–63 °C) and low affinity for nitrite (K_s=1 mℳ), a complex layered cell envelope that stains Gram positive, and uncommon membrane lipids composed of 1,2-diols distinguish N. hollandicus from all other known nitrite oxidizers. N. hollandicus grows on nitrite and CO₂, and is able to use formate as a source of energy and carbon. Genome sequencing and analysis of N. hollandicus revealed the presence of all genes required for CO₂ fixation by the Calvin cycle and a nitrite oxidoreductase (NXR) similar to the NXR forms of the proteobacterial nitrite oxidizers, Nitrobacter and Nitrococcus. Comparative genomic analysis of the nxr loci unexpectedly indicated functionally important lateral gene transfer events between Nitrolancetus and other NOB carrying a cytoplasmic NXR, suggesting that horizontal transfer of the NXR module was a major driver for the spread of the capability to gain energy from nitrite oxidation during bacterial evolution. The surprising discovery of N. hollandicus significantly extends the known diversity of nitrifying organisms and likely will have implications for future research on nitrification in natural and engineered ecosystems.     

Evolutionary history of the Tip100 transposon in the genus Ipomoea

Tip100 is an Ac-like transposable element that belongs to the hAT superfamily. First discovered in Ipomoea purpurea (common morning glory), it was classified as an autonomous element capable of movement within the genome. As Tip100 data were already available in databases, the sequences of related elements in ten additional species of Ipomoea and five commercial varieties were isolated and analyzed. Evolutionary analysis based on sequence diversity in nuclear ribosomal Internal Transcribed Spacers (ITS), was also applied to compare the evolution of these elements with that of Tip100 in the Ipomoea genus. Tip100 sequences were found in I. purpurea, I. nil, I. indica and I. alba, all of which showed high levels of similarity. The results of phylogenetic analysis of transposon sequences were congruent with the phylogenetic topology obtained for ITS sequences, thereby demonstrating that Tip100 is restricted to a particular group of species within Ipomoea. We hypothesize that Tip100 was probably acquired from a common ancestor and has been transmitted vertically within this genus.     

Evolutionary Constraints Favor a Biophysical Model Explaining Hox Gene Collinearity

The Hox gene collinearity enigma has often been approached using models based on biomolecular mechanisms. The biophysical model is an alternative approach based on the hypothesis that collinearity is caused by physical forces pulling the Hox genes from a territory where they are inactive to a distinct spatial domain where they are activated in a step by step manner. Such Hox gene translocations have recently been observed in support of the biophysical model. Genetic engineering experiments, performed on embryonic mice, gave rise to several unexpected mutant expressions that the biomolecular models cannot predict. On the contrary, the biophysical model offers convincing explanation. Evolutionary constraints consolidate the Hox clusters and as a result, denser and well organized clusters may create more efficient physical forces and a more emphatic manifestation of gene collinearity. This is demonstrated by stochastic modeling with white noise perturbing the expression of Hox genes. As study cases the genomes of mouse and amphioxus are used. The results support the working hypothesis that vertebrates have adopted their comparably more compact Hox clustering as a tool needed to develop more complex body structures. Several experiments are proposed in order to test further the physical forces hypothesis.     

Evolutionary analysis of PHLPP1 gene in humans and non-human primates

The chromosome 18q22-23 region has been shown to be implicated in bipolar disorder (BPAD) by several studies. PHLPP1 gene, in the locus (chromosome 18q22-23), is involved in circadian pathways and bears modules like ‘PH domain and leucine rich repeat protein phosphatase’. This gene also contains a polyglutamine (CAG or PolyQ) repeat motif at the carboxyl terminal end. A comparative analysis of the PolyQ repeats of the PHLPP1 gene in humans, non-human primates and other species has been attempted in order to investigate the possible significance of repeat length as seen in other triplet-repeat associated diseases. Sequencing of the CAG repeat in humans and in non-human primates revealed that the CAG repeat is not polymorphic in humans; whereas, in other species it shows an area of high variability, both in length and sequence composition. Despite the conservation of circadian clock components in different species, there is remarkable diversity in the protein structure, regulation and biochemical functions of the circadian orthologs. These can be due to specific adaptations in accordance with the physiology of the particular species providing a species-specific biological advantage.     

Experimental studies of adaptive differentiation in Bahamian Anolis lizards

Populations of the lizards Anolis carolinensis and A. sagrei were experimentally introduced onto small islands in the Bahamas. Less than 15 years after introduction, we investigated whether the populations had diverged and, if so, whether differentiation was related to island vegetational characteristics or propagule size. No effect of founding population size was evident, but differentiation of A. sagrei appears to have been adaptive, a direct relationship existed between how vegetationally different an experimental island was from the source island and how much the experimental population on that island had diverged morphologically. Populations of A. carolinensis had also diverged, but were too few for quantitative comparisons. A parallel exists between the divergence of experimental populations of A. sagrei and the adaptive radiation of Anolis lizards in the Greater Antilles; in both cases, relative hindlimb length and perch diameter are strongly correlated. This differentiation could have resulted from genetic change or environmentally-driven phenotypic plasticity. Laboratory studies on A. sagrei from a population in Florida indicate that hindlimb length exhibits adaptive phenotypic plasticity. Further studies are required to determine if the observed differences among the experimental populations are the result of such plasticity. Regardless of whether the differences result from plasticity, genetic change, or both, the observation that anole populations differentiate rapidly and adaptively when exposed to novel environmental conditions has important implications for understanding the adaptive radiation of Caribbean anoles.     

The parasites of Anolis lizards in the northern Lesser Antilles

Summary The helminth communities from ten species of lizard on seven islands in the Caribbean were sampled by collecting one hundred specimens of each species. Nine genera of parasites were identified; these included six nematodes, two digeneans and an acanthocephalan. No relationship was discernible between parasite density or abundance and island area or altitude, although dry islands tend to have fewer species of parasites. Anolis lizards of the bimaculatus and wattsi series share similar parasites with four out of nine species common to both series. The parasite community of lizards on these islands is depauperate with respect to similar surveys on the larger islands of the Greater Antilles.On three of the islands lizards were sub-sampled by collecting from moist woodland and more xeric habitats. These data suggest that differences between habitats are as significant as differences between islands in determining parasite burdens. Worm burdens of the commonest parasite species, T. cubensis, increased monotonically with host body size and no evidence was found to suggest that these parasites affect either host survival or fecundity. The sex-ratio of this species correlated with mean abundance of the parasite, with females the dominant sex on islands or in habitats where the parasite was common. This pattern may reflect haplodiploid sexual determination in this species.     

Endogeic earthworms shape bacterial functional communities and affect organic matter mineralization in a tropical soil

Priming effect (PE) is defined as a stimulation of the mineralization of soil organic matter (SOM) following a supply of fresh organic matter. This process can have important consequences on the fate of SOM and on the management of residues in agricultural soils, especially in tropical regions where soil fertility is essentially based on the management of organic matter. Earthworms are ecosystem engineers known to affect the dynamics of SOM. Endogeic earthworms ingest large amounts of soil and assimilate a part of organic matter it contains. During gut transit, microorganisms are transported to new substrates and their activity is stimulated by (i) the production of readily assimilable organic matter (mucus) and (ii) the possible presence of fresh organic residues in the ingested soil. The objective of our study was to see (i) whether earthworms impact the PE intensity when a fresh residue is added to a tropical soil and (ii) whether this impact is linked to a stimulation/inhibition of bacterial taxa, and which taxa are affected. A tropical soil from Madagascar was incubated in the laboratory, with a ¹³C wheat straw residue, in the presence or absence of a peregrine endogeic tropical earthworm, Pontoscolex corethrurus. Emissions of ¹²CO₂ and ¹³CO₂ were followed during 16 days. The coupling between DNA-SIP (stable isotope probing) and pyrosequencing showed that stimulation of both the mineralization of wheat residues and the PE can be linked to the stimulation of several groups especially belonging to the Bacteroidetes phylum.     

Insects, birds and lizards as pollinators of the largest-flowered Scrophularia of Europe and Macaronesia

Background and Aims

It has traditionally been considered that the flowers of Scrophularia are mainly pollinated by wasps. We studied the pollination system of four species which stand out for their large and showy flowers: S. sambucifolia and S. grandiflora (endemics of the western Mediterranean region), S. trifoliata (an endemic of the Tyrrhenian islands) and S. calliantha (an endemic of the Canary Islands). Our principal aim was to test whether these species were pollinated by birds or showed a mixed pollination system between insects and birds.

Methods

Censuses and captures of insects and birds were performed to obtain pollen load transported and deposited on the stigmas. Also, a qualitative and quantitative analysis of the flowers and inflorescences was carried out.

Key Results

Flowers were visited by Hymenoptera and by passerine birds. The Canarian species was the most visited by birds, especially by Phylloscopus canariensis, and its flowers were also accessed by juveniles of the lizard Gallotia stehlini. The most important birds in the other three species were Sylvia melanocephala and S. atricapilla. The most important insect-functional groups in the mixed pollination system were: honey-bees and wasps in S. sambucifolia; bumble-bees and wasps in S. grandiflora; wasps in S. trifoliata; and a small bee in S. calliantha.

Conclusions

The species studied show a mixed pollination system between insects and passerine birds. In S. calliantha there is, in addition, a third agent (juveniles of Gallotia stehlini). The participation of birds in this mixed pollination system presents varying degrees of importance because, while in S. calliantha they are the main pollinators, in the other species they interact to complement the insects which are the main pollinators. A review of different florae showed that the large showy floral morphotypes of Scrophularia are concentrated in the western and central Mediterranean region, Macaronesia and USA (New Mexico).     

Evolutionary patchwork of an insecticidal toxin shared between plant-associated pseudomonads and the insect pathogens Photorhabdus and Xenorhabdus

Background

Root-colonizing fluorescent pseudomonads are known for their excellent abilities to protect plants against soil-borne fungal pathogens. Some of these bacteria produce an insecticidal toxin (Fit) suggesting that they may exploit insect hosts as a secondary niche. However, the ecological relevance of insect toxicity and the mechanisms driving the evolution of toxin production remain puzzling.

Results

Screening a large collection of plant-associated pseudomonads for insecticidal activity and presence of the Fit toxin revealed that Fit is highly indicative of insecticidal activity and predicts that Pseudomonas protegens and P. chlororaphis are exclusive Fit producers. A comparative evolutionary analysis of Fit toxin-producing Pseudomonas including the insect-pathogenic bacteria Photorhabdus and Xenorhadus, which produce the Fit related Mcf toxin, showed that fit genes are part of a dynamic genomic region with substantial presence/absence polymorphism and local variation in GC base composition. The patchy distribution and phylogenetic incongruence of fit genes indicate that the Fit cluster evolved via horizontal transfer, followed by functional integration of vertically transmitted genes, generating a unique Pseudomonas-specific insect toxin cluster.

Conclusions

Our findings suggest that multiple independent evolutionary events led to formation of at least three versions of the Mcf/Fit toxin highlighting the dynamic nature of insect toxin evolution.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1763-2) contains supplementary material, which is available to authorized users.     

Evolutionary rescue and adaptation to abrupt environmental change depends upon the history of stress

Whether evolution will be rapid enough to rescue declining populations will depend upon population size, the supply of genetic variation, the degree of maladaptation and the historical direction of selection. We examined whether the level of environmental stress experienced by a population prior to abrupt environmental change affects the probability of evolutionary rescue (ER). Hundreds of populations of two species of yeast, Saccharomyces cerevisiae and Saccharomyces paradoxus were exposed to a range of sublethal concentrations of salt for approximately a hundred generations before transfer to a concentration of salt lethal to the ancestor (150 g l^–1 NaCl). The fitness of surviving populations of both species was a quadratic function of yield: fitness was greatest for large populations that had been selected on low salt concentrations (less than 20 g l⁻¹ NaCl) and small populations that had adapted to high salt (more than 80 g l⁻¹ NaCl). However, differences occurred between species in the probability of ER. The frequency of ER was positively correlated with salt concentration for S. cerevisiae, but negatively correlated with salt concentration in S. paradoxus. These results not only demonstrate that past environmental conditions can determine the probability of ER after abrupt environmental change, but also suggest that there may even be differences between closely related species that are worth further exploration.     

Evolutionary history of mitogen-activated protein kinase (MAPK) genes in Lotus,Medicago, and Phaseolus

Mitogen-Activated Protein Kinase (MAPK) genes encode proteins that mediate various signaling pathways associated with biotic and abiotic stress responses in eukaryotes. The MAPK genes form a 3-tier signal transduction cascade between cellular stimuli and physiological responses. Recent identification of soybean MAPKs and availability of genome sequences from other legume species allowed us to identify their MAPK genes. The main objectives of this study were to identify MAPKs in 3 legume species, Lotus japonicus, Medicago truncatula, and Phaseolus vulgaris, and to assess their phylogenetic relationships. We used approaches in comparative genomics for MAPK gene identification and named the newly identified genes following Arabidopsis MAPK nomenclature model. We identified 19, 18, and 15 MAPKs and 7, 4, and 9 MAPKKs in the genome of Lotus japonicus, Medicago truncatula, and Phaseolus vulgaris, respectively. Within clade placement of MAPKs and MAPKKs in the 3 legume species were consistent with those in soybean and Arabidopsis. Among 5 clades of MAPKs, 4 founder clades were consistent to MAPKs of other plant species and orthologs of MAPK genes in the fifth clade-"Clade E" were consistent with those in soybean. Our results also indicated that some gene duplication events might have occurred prior to eudicot-monocot divergence. Highly diversified MAPKs in soybean relative to those in 3 other legume species are attributable to the polyploidization events in soybean. The identification of the MAPK genes in the legume species is important for the legume crop improvement; and evolutionary relationships and functional divergence of these gene members provide insights into plant genome evolution.