A Molecular Phylogeny of Plesiorycteropus Reassigns the Extinct Mammalian Order ‘Bibymalagasia’

Madagascar is well known for its diverse fauna and flora, being home to many species not found anywhere else in the world. However, its biodiversity in the recent past included a range of extinct enigmatic fauna, such as elephant birds, giant lemurs and dwarfed hippopotami. The ‘Malagasy aardvark’ (Plesiorycteropus) has remained one of Madagascar’s least well-understood extinct species since its discovery in the 19^th century. Initially considered a close relative of the aardvark (Orycteropus) within the order Tubulidentata, more recent morphological analyses challenged this placement on the grounds that the identifiably derived traits supporting this allocation were adaptations to digging rather than shared ancestry. Because the skeletal evidence showed many morphological traits diagnostic of different eutherian mammal orders, they could not be used to resolve its closest relatives. As a result, the genus was tentatively assigned its own taxonomic order ‘Bibymalagasia’, yet how this order relates to other eutherian mammal orders remains unclear despite numerous morphological investigations. This research presents the first known molecular sequence data for Plesiorycteropus, obtained from the bone protein collagen (I), which places the ‘Malagasy aardvark’ as more closely related to tenrecs than aardvarks. More specifically, Plesiorycteropus was recovered within the order Tenrecoidea (golden moles and tenrecs) within Afrotheria, suggesting that the taxonomic order ‘Bibymalagasia’ is obsolete. This research highlights the potential for collagen sequencing in investigating the phylogeny of extinct species as a viable alternative to ancient DNA (aDNA) sequencing, particularly in cases where aDNA cannot be recovered.     

Dark extinction: the problem of unknown historical extinctions

The extinction of species before they are discovered and named (dark extinction, DE) is widely inferred as a significant part of species loss in the ‘pre-taxonomic’ period (approx. 1500–1800 CE) and, to some extent, in the ‘taxonomic period’ (approx. 1800–present) as well. The discovery of oceanic islands and other pristine habitats by European navigators and the consequent introduction of destructive mammals, such as rats and goats, started a process of anthropogenic extinction. Much ecosystem change happened before systematic scientific recording, so has led to DE. Statistical methods are available to robustly estimate DE in the ‘taxonomic period’. For the ‘pre-taxonomic period’, simple extrapolation can be used. The application of these techniques to world birds, for example, suggests that approximately 56 DEs occurred in the ‘taxonomic period’ (1800–present) and approximately 180 in the ‘pre-taxonomic period’ (1500–1800). Targeting collection activities in extinction hotspots, to make sure organisms are represented in collections before their extinction, is one way of reducing the number of extinct species without a physical record (providing that collection efforts do not themselves contribute to species extinction).     

Bacterial genospecies that are not ecologically coherent: population genomics of Rhizobium leguminosarum

Biological species may remain distinct because of genetic isolation or ecological adaptation, but these two aspects do not always coincide. To establish the nature of the species boundary within a local bacterial population, we characterized a sympatric population of the bacterium Rhizobium leguminosarum by genomic sequencing of 72 isolates. Although all strains have 16S rRNA typical of R. leguminosarum, they fall into five genospecies by the criterion of average nucleotide identity (ANI). Many genes, on plasmids as well as the chromosome, support this division: recombination of core genes has been largely within genospecies. Nevertheless, variation in ecological properties, including symbiotic host range and carbon-source utilization, cuts across these genospecies, so that none of these phenotypes is diagnostic of genospecies. This phenotypic variation is conferred by mobile genes. The genospecies meet the Mayr criteria for biological species in respect of their core genes, but do not correspond to coherent ecological groups, so periodic selection may not be effective in purging variation within them. The population structure is incompatible with traditional ‘polyphasic taxonomy′ that requires bacterial species to have both phylogenetic coherence and distinctive phenotypes. More generally, genomics has revealed that many bacterial species share adaptive modules by horizontal gene transfer, and we envisage a more consistent taxonomic framework that explicitly recognizes this. Significant phenotypes should be recognized as ‘biovars'' within species that are defined by core gene phylogeny.     

Disruptive ecological selection on a mating cue

Adaptation to divergent ecological niches can result in speciation. Traits subject to disruptive selection that also contribute to non-random mating will facilitate speciation with gene flow. Such ‘magic’ or ‘multiple-effect’ traits may be widespread and important for generating biodiversity, but strong empirical evidence is still lacking. Although there is evidence that putative ecological traits are indeed involved in assortative mating, evidence that these same traits are under divergent selection is considerably weaker. Heliconius butterfly wing patterns are subject to positive frequency-dependent selection by predators, owing to aposematism and Müllerian mimicry, and divergent colour patterns are used by closely related species to recognize potential mates. The amenability of colour patterns to experimental manipulation, independent of other traits, presents an excellent opportunity to test their role during speciation. We conducted field experiments with artificial butterflies, designed to match natural butterflies with respect to avian vision. These were complemented with enclosure trials with live birds and real butterflies. Our experiments showed that hybrid colour-pattern phenotypes are attacked more frequently than parental forms. For the first time, we demonstrate disruptive ecological selection on a trait that also acts as a mating cue.     

Disturbance Alters the Phylogenetic Composition and Structure of Plant Communities in an Old Field System

The changes in phylogenetic composition and structure of communities during succession following disturbance can give us insights into the forces that are shaping communities over time. In abandoned agricultural fields, community composition changes rapidly when a field is plowed, and is thought to reflect a relaxation of competition due to the elimination of dominant species which take time to re-establish. Competition can drive phylogenetic overdispersion, due to phylogenetic conservation of ‘niche’ traits that allow species to partition resources. Therefore, undisturbed old field communities should exhibit higher phylogenetic dispersion than recently disturbed systems, which should be relatively ‘clustered’ with respect to phylogenetic relationships. Several measures of phylogenetic structure between plant communities were measured in recently plowed areas and nearby ‘undisturbed’ sites. There was no difference in the absolute values of these measures between disturbed and ‘undisturbed’ sites. However, there was a difference in the ‘expected’ phylogenetic structure between habitats, leading to significantly lower than expected phylogenetic diversity in disturbed plots, and no difference from random expectation in ‘undisturbed’ plots. This suggests that plant species characteristic of each habitat are fairly evenly distributed on the shared species pool phylogeny, but that once the initial sorting of species into the two habitat types has occurred, the processes operating on them affect each habitat differently. These results were consistent with an analysis of correlation between phylogenetic distance and co-occurrence indices of species pairs in the two habitat types. This study supports the notion that disturbed plots are more clustered than expected, rather than ‘undisturbed’ plots being more overdispersed, suggesting that disturbed plant communities are being more strongly influenced by environmental filtering of conserved niche traits.     

Helminth Communities of Owls (Strigiformes) Indicate Strong Biological and Ecological Differences from Birds of Prey (Accipitriformes and Falconiformes) in Southern Italy

We compared the helminth communities of 5 owl species from Calabria (Italy) and evaluated the effect of phylogenetic and ecological factors on community structure. Two host taxonomic scales were considered, i.e., owl species, and owls vs. birds of prey. The latter scale was dealt with by comparing the data here obtained with that of birds of prey from the same locality and with those published previously on owls and birds of prey from Galicia (Spain). A total of 19 helminth taxa were found in owls from Calabria. Statistical comparison showed only marginal differences between scops owls (Otus scops) and little owls (Athene noctua) and tawny owls (Strix aluco). It would indicate that all owl species are exposed to a common pool of ‘owl generalist’ helminth taxa, with quantitative differences being determined by differences in diet within a range of prey relatively narrow. In contrast, birds of prey from the same region exhibited strong differences because they feed on different and wider spectra of prey. In Calabria, owls can be separated as a whole from birds of prey with regard to the structure of their helminth communities while in Galicia helminths of owls represent a subset of those of birds of prey. This difference is related to the occurrence in Calabria, but not Galicia, of a pool of ‘owl specialist’ species. The wide geographical occurrence of these taxa suggest that local conditions may determine fundamental differences in the composition of local communities. Finally, in both Calabria and Galicia, helminth communities from owls were species-poor compared to those from sympatric birds of prey. However, birds of prey appear to share a greater pool of specific helmith taxa derived from cospeciation processes, and a greater potential exchange of parasites between them than with owls because of phylogenetic closeness.     

Mimics without models: causes and consequences of allopatry in Batesian mimicry complexes

Batesian mimicry evolves when a palatable species (the ‘mimic’) co-opts a warning signal from a dangerous species (the ‘model’) and thereby deceives its potential predators. Longstanding theory predicts that this protection from predation should break down where the model is absent. Thus, mimics are expected to only co-occur with their model. Yet, many mimics violate this prediction and occur in areas where their model is absent. Here, we discuss the causes and consequences of such allopatric mimics. We also describe how these ‘rule-bending’ mimics provide critical insights into diverse topics ranging from how Batesian mimicry evolves to its possible role in speciation.     

Macrogenomic Evidence for the Origin of the Black Fly Simulium suzukii (Diptera: Simuliidae) on Okinawa Island,Japan

To determine the geographic origin of the black fly Simulium suzukii on Okinawa Island, Japan, macrogenomic profiles derived from its polytene chromosomes were compared with those of mainland and other insular populations of S. suzukii and of the isomorphic Simulium tani species complex. The Okinawan population is a chromosomally unique cytoform, designated ‘D,’ which is essentially monomorphic and differs by about 27 fixed rearrangements from the chromosomal standard sequence for the subgenus Simulium and by two fixed differences from its nearest known relative, representing the type of S. suzukii, on the main islands of Japan. Chromosomal band sequences revealed two additional, sympatric cytoforms of S. suzukii, designated ‘A’ and ‘B,’ each with species status, in Korea, and a third cytoform, designated ‘C,’ on Hokkaido, Japan. A new cytoform, ‘K,’ of S. tani from Malaysia, representing the type of S. tani, is more closely related to cytoforms in Thailand, as are populations from Taiwan previously treated as S. suzukii but more closely aligned with S. tani and newly recognized as cytoform ‘L’ of the latter nominal species. Rooting of chromosomal band sequences by outgroup comparisons allowed directionality of chromosomal rearrangements to be established, enabling phylogenetic inference of cytoforms. Of 41 macrogenomic rearrangements discovered in the five new cytoforms, four provide evidence for a stepwise origin of the Okinawan population from populations characteristic of the main islands of Japan. The macrogenomic approach applied to black flies on Okinawa Island illustrates its potential utility in defining source areas for other species of flies including those that might pose medical and veterinary risks.     

Using the taxon-specific genes for the taxonomic classification of bacterial genomes

Background

The correct taxonomic assignment of bacterial genomes is a primary and challenging task. With the availability of whole genome sequences, the gene content based approaches appear promising in inferring the bacterial taxonomy. The complete genome sequencing of a bacterial genome often reveals a substantial number of unique genes present only in that genome which can be used for its taxonomic classification.

Results

In this study, we have proposed a comprehensive method which uses the taxon-specific genes for the correct taxonomic assignment of existing and new bacterial genomes. The taxon-specific genes identified at each taxonomic rank have been successfully used for the taxonomic classification of 2,342 genomes present in the NCBI genomes, 36 newly sequenced genomes, and 17 genomes for which the complete taxonomy is not yet known. This approach has been implemented for the development of a tool ‘Microtaxi’ which can be used for the taxonomic assignment of complete bacterial genomes.

Conclusion

The taxon-specific gene based approach provides an alternate valuable methodology to carry out the taxonomic classification of newly sequenced or existing bacterial genomes.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1542-0) contains supplementary material, which is available to authorized users.     

Causes of hatching failure in endangered birds

About 10 per cent of birds'' eggs fail to hatch, but the incidence of failure can be much higher in endangered species. Most studies fail to distinguish between infertility (due to a lack of sperm) and embryo mortality as the cause of hatching failure, yet doing so is crucial in order to understand the underlying problem. Using newly validated techniques to visualize sperm and embryonic tissue, we assessed the fertility status of unhatched eggs of five endangered species, including both wild and captive birds. All eggs were classified as ‘infertile’ when collected, but most were actually fertile with numerous sperm on the ovum. Eggs of captive birds had fewer sperm and were more likely to be infertile than those of wild birds. Our findings raise important questions regarding the management of captive breeding programmes.     

Rich Pickings Near Large Communal Roosts Favor ‘Gang’ Foraging by Juvenile Common Ravens,Corvus corax

Ravens (Corvus corax) feed primarily on rich but ephemeral carcasses of large animals, which are usually defended by territorial pairs of adults. Non-breeding juveniles forage socially and aggregate in communal winter roosts, and these appear to function as ‘information centers’ regarding the location of the rare food bonanzas: individuals search independently of one another and pool their effort by recruiting each other at roosts. However, at a large raven roost in Newborough on Anglesey, North Wales, some juveniles have been observed recently to forage in ‘gangs’ and to roost separately from other birds. Here we adapt a general model of juvenile common raven foraging behavior where, in addition to the typical co-operative foraging strategy, such gang foraging behavior could be evolutionarily stable near winter raven roosts. We refocus the model on the conditions under which this newly documented, yet theoretically anticipated, gang-based foraging has been observed. In the process, we show formally how the trade off between search efficiency and social opportunity can account for the existence of the alternative social foraging tactics that have been observed in this species. This work serves to highlight a number of fruitful avenues for future research, both from a theoretical and empirical perspective.     

Higher reproductive skew among birds than mammals in cooperatively breeding species

While competition for limited breeding positions is a common feature of group life, species vary widely in the extent to which reproduction is shared among females (‘reproductive skew’). In recent years, there has been considerable debate over the mechanisms that generate variation in reproductive skew, with most evidence suggesting that subordinates breed when dominants are unable to prevent them from doing so. Here, we suggest that viviparity reduces the ability of dominant females to control subordinate reproduction and that, as a result, dominant female birds are more able than their mammal counterparts to prevent subordinates from breeding. Empirical data support this assertion. This perspective may increase our understanding of how cooperative groups form and are stabilized in nature.     

Experimental evidence for limited vocal recognition in a wild primate: implications for the social complexity hypothesis

Although monitoring social information is a key aspect of the social complexity hypothesis, surprisingly little work has compared social knowledge across different species of wild animals. In the present study, I use playback experiments to test for individual recognition in wild male geladas (Theropithecus gelada) to compare with published accounts of social knowledge in chacma baboons (Papio ursinus). Geladas and baboons are closely related primates living in socially complex groups that differ dramatically in group size—geladas routinely associate with more than 10 times the number of conspecifics than do baboons. Using grunts from non-rival males to simulate approaches, I examined the strength of a subject male''s response when the ‘approach’ was from the direction of (i) non-rival males (control), or (ii) rival males (a more salient stimulus if playback grunts are not recognized by the subject). I compared responses separately based on the degree of social overlap between the caller and the subject. Responses indicate that male geladas, unlike baboons, do not use vocalizations to recognize all of the individuals they regularly encounter. This represents, to my knowledge, the first documented evidence of ‘missing’ social knowledge in a natural primate population. The sharp distinction between baboons and geladas suggests that geladas are either unable or unmotivated to keep track of the individual identity of other males in their multi-level society—even males with whom they have a large degree of social overlap. Thus, these results are consistent with the central assumption of the social complexity hypothesis that social cognition is costly.     

Sexual deception in a cannibalistic mating system? Testing the Femme Fatale hypothesis

Animal communication theory holds that in order to be evolutionarily stable, signals must be honest on average, but significant dishonesty (i.e. deception) by a subset of the population may also evolve. A typical praying mantid mating system involves active mate searching by males, which is guided by airborne sex pheromones in most species for which mate-searching cues have been studied. The Femme Fatale hypothesis suggests that female mantids may be selected to exploit conspecific males as prey if they benefit nutritionally from cannibalism. Such a benefit exists in the false garden mantid Pseudomantis albofimbriata—females use the resources gained from male consumption to significantly increase their body condition and reproductive output. This study aimed to examine the potential for chemical deception among the subset of females most likely to benefit from cannibalism (poorly fed females). Females were placed into one of four feeding treatments (‘Very Poor’, ‘Poor’, ‘Medium’ and ‘Good’), and males were given the opportunity to choose between visually obscured females in each of the treatments. Female body condition and fecundity varied linearly with food quantity; however, female attractiveness did not. That is, Very Poor females attracted significantly more males than any of the other female treatments, even though these females were in significantly poorer condition, less fecund (in this study) and more likely to cannibalise (in a previous study). In addition, there was a positive correlation between fecundity and attractiveness if Very Poor females were removed from the analysis, suggesting an inherently honest signalling system with a subset of dishonest individuals. This is the first empirical study to provide evidence of sexual deception via chemical cues, and the first to provide support for the Femme Fatale hypothesis.     

Contrasting spatial patterns of taxonomic and functional richness offer insights into potential loss of ecosystem services

Functional and trophic perspectives on patterns of species occurrences have the potential to offer new and interesting insights into a range of spatially explicit problems in ecology and conservation. We present the function–area relationship (FAR) and explore linkages between functional and taxonomic species richness for South African birds. We first used beak morphology to classify a subset of 151 South African bird species into 18 functional groups and calculated both the species–area relationship and the FAR at quarter-degree resolution for South Africa. The relationship between functional and taxonomic richness by cell was quadratic rather than linear, with considerable scatter around the curve. We next looked at the spatial relationships between taxonomic diversity and response diversity (i.e. diversity within functional groups) using an a priori categorization of nearly all South African birds into nine functional groups. The spatial distribution of response richness also showed considerable variation in relation to taxonomic richness. Our results demonstrate a novel approach to linking taxonomic, functional and trophic patterns in space and suggest a way in which conservation planning, which has traditionally had a taxonomic focus, could formally incorporate a more functional and food-web-based approach.     

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.     

One species in eight: DNA barcodes from type specimens resolve a taxonomic quagmire

Each holotype specimen provides the only objective link to a particular Linnean binomen. Sequence information from them is increasingly valuable due to the growing usage of DNA barcodes in taxonomy. As type specimens are often old, it may only be possible to recover fragmentary sequence information from them. We tested the efficacy of short sequences from type specimens in the resolution of a challenging taxonomic puzzle: the Elachista dispunctella complex which includes 64 described species with minuscule morphological differences. We applied a multistep procedure to resolve the taxonomy of this species complex. First, we sequenced a large number of newly collected specimens and as many holotypes as possible. Second, we used all >400 bp examine species boundaries. We employed three unsupervised methods (BIN, ABGD, GMYC) with specified criteria on how to handle discordant results and examined diagnostic bases from each delineated putative species (operational taxonomic units, OTUs). Third, we evaluated the morphological characters of each OTU. Finally, we associated short barcodes from types with the delineated OTUs. In this step, we employed various supervised methods, including distance‐based, tree‐based and character‐based. We recovered 658 bp barcode sequences from 194 of 215 fresh specimens and recovered an average of 141 bp from 33 of 42 holotypes. We observed strong congruence among all methods and good correspondence with morphology. We demonstrate potential pitfalls with tree‐, distance‐ and character‐based approaches when associating sequences of varied length. Our results suggest that sequences as short as 56 bp can often provide valuable taxonomic information. The results support significant taxonomic oversplitting of species in the Elachista dispunctella complex.     

Does Trapping Influence Decision-Making under Ambiguity in White-Lipped Peccary (Tayassu pecari)?

The white-lipped peccary (Tayassu pecari) is an endangered species whose bold anti-predator behaviour in comparison to related species may increase its vulnerability to hunting and predation. We used a judgement bias test to investigate whether captive peccaries that had recently experienced a trapping event made more ‘pessimistic’ decisions under ambiguity. If so, this would indicate (i) that the procedure may induce a negative affective state and hence have welfare implications, and (ii) that the species is able to adopt a cautious response style despite its bold phenotype. Eight individuals were trained to ‘go’ to a baited food bowl when a positive auditory cue (whistle; CS+) was given and to ‘no-go’ when a negative cue (horn A; CS-) was sounded to avoid a loud sound and empty food bowl. An ‘ambiguous’ auditory cue (bell; CSA) was presented to probe decision-making under ambiguity. Individuals were subjected to three tests in the order: T1 (control-no trap), T2 (24h after-trap procedure), and T3 (control-no trap). In each test, each animal was exposed to 10 judgement bias trials of each of the three cue types: CS+,CS-,CS_A. We recorded whether animals reached the food bowl within 60s (‘go’ response) and their response speed (m/s). The animals varied in their responses to the CS_A cue depending on test type. In all tests, animals made more ‘go’ responses to CS+ than CS_A. During control tests (T1 and T3), the peccaries showed higher proportions of ‘go’ responses to CS_A than to CS-. In T2, however, the animals showed similar proportions of ‘go’ responses to CS_A and CS-, treating the ambiguous cue similarly to the negative cue. There were differences in their response speed according to cue type: peccaries were faster to respond to CS+ than to CS- and CS_A. Trapping thus appeared to cause a ‘pessimistic’ judgement bias in peccaries, which may reflect a negative affective state with implications for the welfare and management of captive individuals, and also function to increase caution and survival chances following such an event in the wild environment.