Angus Davison

On the origin of faeces: morphological versus molecular methods for surveying rare carnivores from their scats

Charismatic mammals remain a linchpin in attracting publicity and funds for the conservation of native habitats and organisms. Unfortunately, the same animals are frequently scarce and difficult to survey. For many, confirming their presence through faecal surveys is the only cost-effective approach. Here we show that, contrary to received opinion, expert naturalists fail reliably to distinguish pine marten Martes martes faeces (‘scats’) from those of foxes Vulpes vulpes. Moreover, their judgement fails completely when the animals and their scats are at their most scarce. This unexpected result from such a well-studied species has important implications for the monitoring of endangered mammals. We recommend that in the future, a multi-evidence approach should be adopted to monitor elusive mammals, involving DNA methods, cast hair identification, camera traps, and non-leading ‘sighting’ questionaires. For national surveys, it may soon become cost-effective to screen large numbers of samples using microarray technology.

Mitochondrial phylogeography and population history of pine martens Martes martes compared with polecats Mustela putorius.

The flora and fauna of Europe are linked by a common biogeographic history, most recently the Pleistocene glaciations that restricted the range of most species to southern refugial populations. Changes in population size and migration, as well as selection, have all left a signature on the genetic differentiation. Thus, three paradigms of postglacial recolonization have been described, inferred from the patterns of DNA differentiation. Yet some species, especially wide‐ranging carnivores, exhibit little population structuring between the proposed refugia, although relatively few have been studied due to the difficulty of obtaining samples. Therefore, we investigated mitochondrial variation in pine martens, Martes martes, in order to understand the extent to which they were affected by glacial cycles, and compared the results with an analysis of sequences from polecats, Mustela putorius. A general lack of ancient lineages, and a mismatch distribution that is consistent with an expanding population, is evidence that the present‐day M. martes and Mu. putorius in central and northern Europe colonized from a single European refugium following a recent glaciation. There has also been interspecific mitochondrial introgression between M. martes and the sable M. zibellina in Fennoscandia.

Multilocus genetic models of handedness closely resemble single‐locus models in explaining family data and are compatible with genome‐wide association studies

Right‐ and left‐handedness run in families, show greater concordance in monozygotic than dizygotic twins, and are well described by single‐locus Mendelian models. Here we summarize a large genome‐wide association study (GWAS) that finds no significant associations with handedness and is consistent with a meta‐analysis of GWASs. The GWAS had 99% power to detect a single locus using the conventional criterion of P < 5 × 10−8 for the single locus models of McManus and Annett. The strong conclusion is that handedness is not controlled by a single genetic locus. A consideration of the genetic architecture of height, primary ciliary dyskinesia, and intelligence suggests that handedness inheritance can be explained by a multilocus variant of the McManus DC model, classical effects on family and twins being barely distinguishable from the single locus model. Based on the ENGAGE meta‐analysis of GWASs, we estimate at least 40 loci are involved in determining handedness.

Hybridization and the phylogenetic relationship between polecats and domestic ferrets in Britain

Ferrets (Mustela furo) were domesticated from polecats (M. putorius, M. eversmannii) over 2000 years ago. Following their introduction to Britain, they escaped and hybridized with native European polecats (M. putorius). Native polecats declined to the point of near extinction prior to World War I, but have recently begun to expand from a Welsh refugium. Concern has arisen as to the extent of polecat/ferret introgression, and in particular, whether the expanding population is of mainly hybrid origin. Therefore, mitochondrial DNA sequencing was used to investigate polecat genetic diversity in Britain. Two geographically distinct lineages were found, where one may be ancestral to the British polecat, and the other to the domestic ferret. The ancestral distribution of each lineage, or assortative mating is sufficient to explain the observed pattern. A further comparison between the distribution of the polecat phenotype and mitochondrial haplotype implies that the current population expansion may be mediated by dispersing male polecats hybridizing with female feral ferrets. However, the wild source of the ferret remains obscure. Relatively recent speciation from European mink (M. lutreola) and black-footed ferrets (M. nigripes), and/or the effects of hybridization result in an unresolved molecular phylogeny.

The convoluted evolution of snail chirality

The direction that a snail (Mollusca: Gastropoda) coils, whether dextral (right-handed) or sinistral (left-handed), originates in early development but is most easily observed in the shell form of the adult. Here, we review recent progress in understanding snail chirality from genetic, developmental and ecological perspectives. In the few species that have been characterized, chirality is determined by a single genetic locus with delayed inheritance, which means that the genotype is expressed in the mothers offspring. Although research lags behind the studies of asymmetry in the mouse and nematode, attempts to isolate the loci involved in snail chirality have begun, with the final aim of understanding how the axis of left–right asymmetry is established. In nature, most snail taxa (>90%) are dextral, but sinistrality is known from mutant individuals, populations within dextral species, entirely sinistral species, genera and even families. Ordinarily, it is expected that strong frequency-dependent selection should act against the establishment of new chiral types because the chiral minority have difficulty finding a suitable mating partner (their genitalia are on the ‘wrong’ side). Mixed populations should therefore not persist. Intriguingly, however, a very few land snail species, notably the subgenus Amphidromus sensu stricto, not only appear to mate randomly between different chiral types, but also have a stable, within-population chiral dimorphism, which suggests the involvement of a balancing factor. At the other end of the spectrum, in many species, different chiral types are unable to mate and so could be reproductively isolated from one another. However, while empirical data, models and simulations have indicated that chiral reversal must sometimes occur, it is rarely likely to lead to so-called ‘single-gene’ speciation. Nevertheless, chiral reversal could still be a contributing factor to speciation (or to divergence after speciation) when reproductive character displacement is involved. Understanding the establishment of chirality, the preponderance of dextral species and the rare instances of stable dimorphism is an important target for future research. Since the genetics of chirality have been studied in only a few pulmonate species, we also urge that more taxa, especially those from the sea, should be investigated.

History or current selection? A molecular analysis of 'area effects' in the land snail Cepaea nemoralis

We have used molecular variation in microsatellite and mitochondrial DNA to throw light on the origins of enigmatic geographical patterns, known as ‘area effects’, in the shell polymorphisms of the land snail Cepaea nemoralis. Our aim was to assess the relative importance of recent selection and historical events in the formation of these patterns. On the Marlborough Downs in Wiltshire, England, the ‘type locality’ for area effects, the frequencies of microsatellites are significantly associated with the frequencies of alleles for shell banding. A less clear association is found between microsatellites and shell colour. Mitochondrial haplotypes show no significant relationships. Although the correlated geographical patterns could be the results of random genetic drift from an initially uniform array of populations, the magnitudes of the patterns, and of the correlations between them, seem too strong to have arisen by drift since the last glaciation. Our results suggest that invasions from refugia have been the most important factors in forming area effects.

Land snails as a model to understand the role of history and selection in the origins of biodiversity

Abstract It is nearly 100 years since the first studies on variation in the shell patterns of land snails. Subsequently, snails have come to play an important role in our understanding of natural selection in the wild. In particular, snails have been an ideal model to understand the roles of history and selection in the origins of diversity. More recently, many studies have investigated the molecular genetic variation within snails. It is clear that snails are unusual, because some genes may vary by 10%–30% within a species. This molecular variation affords an excellent opportunity to further understand the action of natural selection in shaping the present-day phenotypic diversity. In the first part of this review, I illustrate the distinction between the historical and selective interpretations using one of the best-studied species, Cepaea nemoralis, and the example of “area effects.” In the second part, studies that have compared patterns of morphological and molecular variation (especially DNA) are examined.

DNA barcoding of stylommatophoran land snails: a test of existing sequences

DNA barcoding has attracted attention because it is a potentially simple and universal method for taxonomic assignment. One anticipated problem in applying the method to stylommatophoran land snails is that they frequently exhibit extreme divergence of mitochondrial DNA sequences, sometimes reaching 30% within species. We therefore trialled the utility of barcodes in identifying land snails, by analysing the stylommatophoran cytochrome oxidase subunit I sequences from GenBank. Two alignments of 381 and 228 base pairs were used to determine potential error rates among a test data set of 97 or 127 species, respectively. Identification success rates using neighbour‐joining phylogenies were 92% for the longer sequence and 82% for the shorter sequence, indicating that a high degree of mitochondrial variation may actually be an advantage when using phylogeny‐based methods for barcoding. There was, however, a large overlap between intra‐ and interspecific variation, with assignment failure (per cent of samples not placed with correct species) particularly associated with a low degree of mitochondrial variation (Kimura 2‐parameter distance < 0.05) and a small GenBank sample size (< 25 per species). Thus, while the optimum intra/interspecific threshold value was 4%, this was associated with an overall error of 32% for the longer sequences and 44% for the shorter sequences. The high error rate necessitates that barcoding of land snails is a potentially useful method to discriminate species of land snail, but only when a baseline has first been established using conventional taxonomy and sample DNA sequences. There is no evidence for a barcoding gap, ruling out species discovery based on a threshold value alone.

The evolution of extreme shell shape variation in the land snail Ainohelix editha: a phylogeny and hybrid zone analysis

Ainohelix editha from Hokkaido, Japan, exhibit great geographical variation in their shell morphology. In particular, A. editha in two quite separate locations, Shimamaki and Samani, are striking because they are extremely flat and have a sharp keel, whereas at adjacent sites the shells are globular or depressed‐globular. We used mitochondrial 16S rRNA and nuclear ITS‐2 sequences to infer a phylogeny among 47 snails from 29 locations. Snails from the two keeled‐flat populations clustered separately in the phylogeny, suggesting that this unusual shell form could have evolved independently. A morphological analysis of shells collected along a transect between keeled‐flat and globular snail sites showed a cline for shell shape and the angle of the keel. Two different mtDNA lineages were found across the transect, with a cline for an ITS‐2 single nucleotide polymorphism. Together, the results may suggest a lack of reproductive isolation between keeled‐flat and globular snails, with possible introgression by hybridization.

Speciation and gene flow between snails of opposite chirality.

Left-right asymmetry in snails is intriguing because individuals of opposite chirality are either unable to mate or can only mate with difficulty, so could be reproductively isolated from each other. We have therefore investigated chiral evolution in the Japanese land snail genus Euhadra to understand whether changes in chirality have promoted speciation. In particular, we aimed to understand the effect of the maternal inheritance of chirality on reproductive isolation and gene flow. We found that the mitochondrial DNA phylogeny of Euhadra is consistent with a single, relatively ancient evolution of sinistral species and suggests either recent “single-gene speciation” or gene flow between chiral morphs that are unable to mate. To clarify the conditions under which new chiral morphs might evolve and whether single-gene speciation can occur, we developed a mathematical model that is relevant to any maternal-effect gene. The model shows that reproductive character displacement can promote the evolution of new chiral morphs, tending to counteract the positive frequency-dependent selection that would otherwise drive the more common chiral morph to fixation. This therefore suggests a general mechanism as to how chiral variation arises in snails. In populations that contain both chiral morphs, two different situations are then possible. In the first, gene flow is substantial between morphs even without interchiral mating, because of the maternal inheritance of chirality. In the second, reproductive isolation is possible but unstable, and will also lead to gene flow if intrachiral matings occasionally produce offspring with the opposite chirality. Together, the results imply that speciation by chiral reversal is only meaningful in the context of a complex biogeographical process, and so must usually involve other factors. In order to understand the roles of reproductive character displacement and gene flow in the chiral evolution of Euhadra, it will be necessary to investigate populations in which both chiral morphs coexist.