Genetic relatedness assessment through individual odour similarities in mice

Previous research has demonstrated that closer genetic relatedness between individuals (from kin to across species) is associated with greater similarity in the qualities of their individual odours ('odour-genes covariance'). This predictable relationship between individual genotypes and individual odours could enable animals to assess their degree of genetic relatedness to other individuals by comparing the degree of similarity between another individual's odour and their own odour. In two-choice tests with odours of unfamiliar mice from different populations and species, subjects from two species of wild mice, Mus spicilegus and M. musculus , that had been raised in mixed litters of both species spent significantly more time investigating the ano-genital odour of the more genetically similar individual. This differential interest was not affected by common rearing with heterospecifics. These responses are consistent with a self-referencing mechanism enabling differential responses across a wide spectrum of genetic relatedness from kin through populations to heterospecifics. These assessments depend on the degree of similarity between the donor's and the subject's odours rather than on differences between them. Such a parsimonious mechanism may provide a basis for differential responses to conspecifics as opposed to heterospecifics that may function as a premating isolating mechanism.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 78, 595–603.     

Reliability of odour–genes covariance despite diet changes: a test in mound‐building mice

Odour–genes covariance (i.e. that individual odour similarities covary with genetic similarity) allows animals to assess their genetic relatedness to one another by comparing the similarities between their individual odours. The reliability of the odour–gene covariance phenomenon under environmental changes has not yet been explored. Using an innovative habituation‐generalization procedure, we tested whether the modifications of body odours induced by a change in diet interfered with the perceived similarity of individual odours of more genetically similar individuals. The effects of a change in diet, by adding aniseed flavour to the drinking water, was assessed in male mound‐building mice, a species in which odour–genes covariance has already been demonstrated. The results obtained indicate that mice perceive more similarities in the odours of sibling males than in those of nonrelatives, despite the effects of diet on body odours. We suggest that the reliability of signals arising from odour–genes covariance is likely a result of the independence between traits indicating genetic relatedness and indicator signals of biological states (e.g. diet) in body odours. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 682–688.     

Odour-genes eovariance and differential investigation of individual odours in the Mus species complex

Previous research using habituation techniques has demonstrated that greater genetic similarity between two individuals is associated with more similarity in the qualities of their individual odours ('odour-genes eovariance'). We assessed odour similarities across species in two pairs of genetically close species within the Mus species complex (M. musculus and M. domesticus; M. spicilegus and M. macedonicus). Subjects treated odours within each species pair as similar compared with an odour from the other species pair. Subjects also treated odours of M. spicilegus males from the same population as similar compared with the odour of M. spicilegus males from a different population. This confirms odour-genes eovariance across species and within populations and also supports previous findings that odour similarities are more salient than specific odour markers. When adult males were presented with odours of females from two different heterospecific species, subjects spent more time investigating the odour from his own species pair than the other species pair, indicating greater interest in the odour of the closer heterospecific and demonstrating that odour-genes eovariance is reflected in behavioural responses to odours. Implications of odour-genes eovariance as a basis for identifying degrees of genetic relatedness of unfamiliar individuals through similarities in individual odours are discussed.     

Individual odour similarities across species parallel phylogenetic relationships in the S. ehrenbergi superspecies of mole-rats

Research using habituation techniques has shown that rodents from the same kin group, population, or species share similarities in their individual odours that covary with shared genetic similarities between them, that is, the closer their genetic relatedness, the more similar their odours. We assessed similarities in individual odours across four sibling species of subterranean mole-rats from the Spalax ehrenbergi superspecies in Israel. Mole-rats were habituated to the urine odour of a same-sex individual from one species then tested with urine odours of individuals from two different species of the superspecies. Subjects treated urine odours of individuals from more closely genetically related species as similar compared with the odours of individuals from a less closely related species, showing that the covariance between odours and genes extends across species. These similarities in odour also paralleled genetic similarities determined by molecular analysis: odours of descendent species were perceived as similar to those of their closest ancestral species, suggesting that some qualities of the odour of the ancestral species persist in the descendent species. It is generally assumed that during speciation incipient species develop species-specific markers, including, for example, odour markers, to facilitate discrimination of conspecifics from close ancestral heterospecifics. Our findings indicate that similarities in odours across species are more salient than species-specific odour markers. Such findings may also have important implications for mechanisms of species recognition. Copyright 2000 The Association for the Study of Animal Behaviour.     

Individual Odour Similarity and Discrimination in the Coruro (Spalacopus cyanus, Octodontidae)

Previous studies of subterranean, fossorial and above‐ground rodents have demonstrated that similarities in individual odours covary with genetic similarities thus supporting the theory of odour‐genes covariance (i.e. the closer the individuals are genetically, the greater the similarities between their odours). We used the habituation‐generalization paradigm, where the subject is exposed to the same odour stimulus in three consecutive habituation trials followed by two test trials in which the odour from two other individuals are presented successively. Using this test design, we showed that the socially living coruros (Spalacopus cyanus) discriminate individuals on the basis of their ano‐genital odours and also respond to odour similarities between individuals. Male and female subjects treated ano‐genital odours of two same‐sex family members and also the odours of two sibling strangers as different to each other. At the same time, they treated the odours of siblings as similar compared with the odour of an unrelated individual. No gender differences were detected. Our results contrast with those from other rodent species that did not spontaneously discriminate between individual odours of siblings from a different family than their own. The polygyneous lifestyle may provide the selective background for that difference. Additional research will be necessary to explore this hypothesis and to rule out differences due to dietary preferences and due to the type of paradigm chosen for the tests.     

Low population genetic structuring of two cryptic bat species suggests their migratory behaviour in continental Europe

Although two cryptic pipistrelle bat species, Pipistrellus pipistrellus and Pipistrellus pygmaeus , belong among the most common bat species in Europe, it is still unclear whether they can migrate over long distances between summer and winter roosts. Long-distance migratory species may be expected to show low levels of genetic structuring in large areas due to regular mixing of the gene pool by mating that occurs during migration and/or hibernation. Conversely, the dispersal of gametes in sedentary species is spatially restricted, populations are more genetically structured, and isolation by relatively short distance is visible. By analysing diversity of highly variable microsatellites within and among summer colonies of both studied species in central Europe, we found that differentiation between populations is very weak. Both classical F _ST and Bayesian clustering approach failed to detect genetic structure among colonies and there was no significant isolation-by-distance pattern. The analyses of relatedness, however, revealed that individuals within colonies are more related than random suggesting philopatry of at least one sex. The results were very similar for the two species. The high level of gene flow among central European populations, even on large geographic distances, is discussed in relation with migrations, dispersal, and mating behaviour.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 103–114.     

Trends in floral scent chemistry in pollination syndromes: floral scent composition in hummingbird-pollinated taxa

We studied an assemblage of 17 species of bird-pollinated Ecuadorian plants (from 14 angiosperm families), including taxa pollinated by short-billed (trochiline) and sickle-billed (hermit) hummingbirds. Hummingbirds are widely supposed to ignore fragrance while visiting flowers. We collected floral headspace odours in order to test the general prediction that specialist hummingbird-pollinated flowers are scentless. In nine out of 17 of these species we failed to detect any odours using gas chromatography-mass spectrometry (GC-MS), whereas the remaining eight species produced trace levels of volatile compounds. Most of these odour compounds were of terpenoid or lipoxygenase derivation and are commonly emitted by vegetative as well as floral plant tissues. Further studies will be required to determine whether these weak odours attract alternative pollinators, repel enemies or represent vestiges of a scented ancestry.  © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society , 2004, 146 , 191–199.     

Biogeographical connections between the Maghreb and the Mediterranean peninsulas of southern Europe

The glacial–interglacial cycles have caused severe range modifications of species' distributions. In Europe, thermophilic species had to retreat into geographically distinct southern refugia during glaciations. This process produced strong genetic imprints, which are still detectable by the present pattern of genetic differentiation and the distribution of regional diversity. To reveal the biogeographical imprints in the western Mediterranean, we analysed 26 populations of the butterfly Maniola jurtina spread over large areas of its European and North African distribution range. The samples were analysed using allozyme electrophoresis. We detected three genetic groups, divided into Western Europe, Central/Eastern Europe, and Italy with the Maghreb. The North African samples randomly cluster within the Italian samples. Even the population sampled in Morocco is genetically closely related to these samples and not to the geographically neighbouring Iberian ones. Parameters of genetic diversity showed similar values over the whole study area. The observed genetic pattern reflects possible glacial refugia in Europe located in the Iberian Peninsula and the Balkans. For North Africa and Italy, our data reveal a colonization of Africa originating from Italy.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 693–703.     

Using image analysis on the ventral colour pattern in Salamandrina perspicillata (Amphibia: Salamandridae) to discriminate among populations

The ventral colour pattern in Salamandrina perspicillata is characteristic of each individual and remains invariant throughout the salamanders' life. The present study aimed to determine, using statistical methods applied to quantitative image analysis, whether the coloration pattern is population-specific. The images of ventral colour pattern of 180 salamanders belonging to five populations were analysed. The images were previously warped by geometric morphometry. To our knowledge, this is the first study to use an approach based on geometric morphometrics to standardize ventral shapes. This technique is useful for eliminating form distortions. The results of an analysis of similarities recognized more coloration similarity among individuals of the same population than among individuals from different populations. Analysis by partial least squares correctly classified the 88.88% of individuals into the correct population. The similarities or differences among individuals of different populations are not related to the geographical distances. The results obtained showed that the coloration of the ventral side of the head of the salamanders can be used for discriminating among populations.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 35–43.     

Genetic variation within and between Iliamna corei and I. remota (Malvaceae): implications for species delimitation

Iliamna corei and I. remota are classified as endangered species; however, their designation as separate species has been questioned. In order to address this problem, intersimple sequence repeat (ISSR) data were generated to examine patterns of genetic differentiation within and between these two taxa. ISSRs were used to screen individuals for genetic diversity of I. corei from the single known natural population and two garden populations, and individuals of I. remota from the six natural populations and four garden populations. Using ten primers, 140 informative markers were generated. Ninety-four percent of loci detected revealed polymorphisms. Cluster analysis (neighbour-joining, NJ) revealed that the two species are genetically distinct and that the Illinois populations of I. remota were genetically distinct from the Virginia populations of I. remota . Ordination by Principal Coordinate Analysis (PCoA) supported the findings of the NJ, with a separation of I. corei and I. remota . Analysis of Molecular Variance (AMOVA) revealed that the majority of variation detected was within populations, which is consistent with other self-incompatible plants. The results indicate a correlation between the geographical distributions of the species and gene flow.  © 2006 The Linnean Society of London, Botanical Journal of the Linnean Society , 2006, 151 , 345–354.     

Volatile leaf oil diversity in the narrow range endemic Eucalyptus argutifolia (Myrtaceae) and its widespread congener Eucalyptus obtusiflora

Variation in the qualitative composition of volatile leaf oil was examined in the rare Eucalyptus argutifolia and its widespread congener Eucalyptus obtusiflora . The results revealed that, consistent with the pattern seen with allozymes, E. argutifolia had less variation within populations than E. obtusiflora . Total leaf oil diversity was also significantly lower in the rare species. As found with allozymes, most leaf oil diversity was within populations, but there was also a significant proportion of the variation between populations (25.2% and 27.3% for E. argutifolia and E. obtusiflora , respectively). There were significant associations between phenotypic distance based on leaf oils and geographical distance and between phenotypic and genetic distance across all populations, but these associations were not evident within species. Factors leading to reduced variation in E. argutifolia appear to affect all types of variation, but the relationships between different types of variation within the species are less apparent.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 738–745.     

Parnassia palustris: a genetically diverse species in Scandinavia

Patterns of variation at nine enzyme loci were examined in 528 plants representing diploid and tetraploid populations of Parnassia palustris s. l. in Europe to assess genetic variation patterns and migration history. Half of the plants showed a unique multilocus phenotype and 75% of all phenotypes occurred only in Scandinavia. Diploid populations showed similar levels of genetic diversity as other widespread outbreeding species with animal-mediated pollination and F -statistics indicated excessive heterozygosity and low rates of gene flow among them. In spite of dramatic population histories caused by the ice ages, diploid populations have maintained the same genetic diversity in Scandinavia as in central and southern Europe. Northern populations have apparently been established through the gradual advance of genetically variable populations and patterns of variation at individual loci indicate different migration routes, from the south-south-west and the east-north-east, respectively. The data strongly support a repeated autoploid origin of the tetraploid cytotype which has been much more successful than the diploid progenitors in colonizing new land since the last ice age. High genetic diversity in Scandinavia has apparently been obtained by a combination of immigration of plants from different source areas and recurrent formation of autotetraploids from diploid progenitors.  © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society , 2003, 142 , 347−372.     

Plasticity, its cost, and phenotypic selection under water and nutrient stress in two annual grasses

A comparative approach can prove to be a useful tool for studying phenotypic plasticity, if applied to specific traits involved in adaptation to particular environment in more than one species across co-located populations. The present study tested whether two annual grasses, Hordeum spontaneum and Avena sterilis , belonging to the same guild, having similar stature, seed dispersal mechanism, breeding system, and genetic variation, and sampled in exactly the same environmentally specific locations, differed with respect to: (1) plasticity in traits involved in adaptation, namely the onset of reproduction and maternal investment involving the number of inflorescences, spikelets per inflorescence, the weight of individual spikelets, and abortion rate; (2) the cost of this plasticity, and (3) the pattern of phenotypic selection on the above traits. The two species exhibited highly differing amounts of phenotypic plasticity in the onset of flowering and several reproductive traits (number of inflorescences, spikelets per inflorescence, abortion rate), but no plasticity costs in any experimental environment. The two species demonstrated a decreasing similarity in the regulation of reproduction in four experimental environments: benign, water, nutrients and water × nutrient deficient. Correlational selection appears to contribute, although not solely, to the observed species differences with respect to the regulation of reproduction.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 581–593.     

Do taxonomic divisions reflect genetic differentiation? A comparison of morphological and genetic data in Coenonympha tullia (Müller), Satyrinae

Historically, morphological variation has been used to classify many species (and subspecies) of Lepidoptera. However, some of this variation may be unsuitable for inferring the recent evolutionary history of populations. Genetic data provide an alternative. We examine the morphological and genetic variation within and between British subspecies of Coenonympha tullia (Müller 1764) to test the hypothesis that neutral genetic variation corresponds to morphological variation. We find that most morphological and genetic variation occurs within populations and that those populations designated as subspecies based on morphological characters are not necessarily most closely related for mitochondrial DNA or nuclear DNA (amplified fragment length polymorphisms and allozymes). Thus, the notion that wing spot variation reflects population isolation and therefore genetic differentiation does not hold. The present study highlights the need for genetic data where taxonomy may be based on environmentally plastic or locally adapted characters because such characters will not reflect the true population genetic history.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 314–327.     

Morphotypes,varieties, or subspecies?: genetic diversity and differentiation of four Saintpaulia (Gesneriaceae) morphotypes from the East Usambara Mountains,Tanzania

Saintpaulia (H. Wendl.) is a forest-dependent, endangered plant genus endemic to Tanzania and Kenya. The taxonomy of Saintpaulia from the Usambara Mountains and adjacent lowlands in north-eastern Tanzania is problematic because of the morphological similarity of the species and the presence of considerable intraspecific variation. Conventional molecular phylogenetic methods have failed to reveal the genetic structure of this Saintpaulia complex. In this study, we assessed the genetic composition of 12 Saintpaulia populations, representing four different morphotypes, from the East Usambara Mountains using inter-simple sequence repeat (ISSR) markers. Relatively high genetic diversities were observed within populations (mean h  = 0.320), indicating their adaptive potential. Little genetic differentiation amongst populations (mean F _st  = 0.063) and the genetic divergence of the rosulate and trailing morphotypes support the hypothesis of ongoing divergent evolution within the East Usambara metapopulation(s) of Saintpaulia .  © 2008 The Linnean Society of London, Botanical Journal of the Linnean Society , 2008, 157 , 347–355.     

The genetic structure of crossbills suggests rapid diversification with little niche conservatism

Conservatism of ecological niches can cause geographical ranges or the formation of new species to be constrained, and might be expected in situations where strong trade‐offs result in ecological specialization. Here we address the flexibility of resource use in European crossbills by comparing the ecological and genetic similarities between four Mediterranean and three northern European crossbill populations, all specialized in feeding on a different resource. We used sequence data of one mitochondrial and two nuclear genes from between 211 and 256 individuals. The northern crossbills were genetically too similar to infer which population was more related to the southern ones. Crossbills from the island of Mallorca showed genetic signatures of a stable and isolated population, supporting their past treatment as a locally (co)evolving taxon, and seem to have evolved from an ecologically distinct ancestor. Previous studies in other populations also suggest that genetic similarity does not predict morphological and resource similarity. We estimate that the divergence of all western European crossbills has occurred within the last 11 000 years. Overall, it appears that crossbills can diversify rapidly and with little niche conservatism, but that such potentially reproductively isolated specialists are evolutionarily short‐lived. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 908–922.     

Low population differentiation and high genetic diversity in the invasive species Carduus acanthoides L. (Asteraceae) within its native range in the Czech Republic

Colonizing species are predicted to suffer from reductions in genetic diversity during founding events. Although there is no unique mode of reproduction that is characteristic of successful plant colonizers, many of them are predominantly self-fertilizing or apomictic species, and almost all outcrossing colonizers are self-compatible. Carduus acanthoides comprises a species of disturbed habitats with wind-dispersed seeds that colonizes open spaces of various sizes. Population genetic diversity was expressed by assessing patterns of variation at nine putatively neutral allozyme loci within and among 20 natural populations in its native distribution range in the Czech Republic. Overall, C. acanthoides displayed high levels of genetic diversity compared to other herbaceous plants. The percentage of polymorphic loci was 84.5, with values of 2.37, 0.330, and 0.364 for the mean number of alleles per polymorphic locus ( A ), observed heterozygosity ( H _o), and expected heterozygosity ( H _e), respectively. There was only weak evidence of inbreeding within populations ( f  = 0.097) and very low genetic differentiation among populations ( θ  = 0.085). Analyses of the data provide strong evidence for isolation-by-distance for the whole study area. Even the colonizing species, C. acanthoides , currently supports a substantial amount of allozyme variation at both the species and population levels.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 596–607.     

Impact of ocean barriers, topography, and glaciation on the phylogeography of the catfish Trichomycterus areolatus (Teleostei: Trichomycteridae) in Chile

We examined the role of several earth history events on the phylogeographic distribution of the catfish Trichomycterus areolatus in Chile using the cytochrome b gene. We explored three biogeographic hypotheses: that sea level changes have resulted in the isolation of populations by drainages; that glaciation has impacted genetic diversity; and that ichthyological subprovince boundaries correspond to phylogeographic breaks in our focal species. We found seven well-supported clades within T. areolatus with high levels of genetic divergence. The strongest signal in our data was for an important role of sea level changes structuring populations. Five of the seven clades mapped cleanly to the geographic landscape and breaks corresponded closely to areas of narrowest continental shelf. In addition, few haplotypes were shared between rivers within clades, suggesting that only limited local movement of individuals has occurred. There was no relationship between the levels of genetic diversity and the proportion of individual drainages covered by glaciers during the last glacial maximum. Two phylogeographic breaks within T. areolatus did match the two previously identified faunal boundaries, but we found three additional breaks, which suggests that faunal breaks have only limited utility in explaining phylogeographic patterns. These results imply that the narrow continental shelf coupled with sea level changes had a strong influence on the obligate freshwater fishes in Chile.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 876–892.     

How did an annual plant react to Pleistocene glaciations? Postglacial history of Rhinanthus angustifolius in Europe

The impact of climate fluctuations during the Pleistocene on the geographic structure of genetic variation in plant populations is well documented, but there is a lack of studies of annual species at the European scale. The present study aimed to infer the history of the widespread European annual Rhinanthus angustifolius C. C. Gmelin (Orobanchaceae). We explored variation in chloroplast DNA (cpDNA) sequences and amplified fragment length polymorphism (AFLP) in twenty-nine populations covering the entire distribution area of the species. Five AFLP groups were identified, suggesting at least two glacial refugial areas: one area in southwestern Europe and one large eastern area in the Balkan/Caucasus. Recolonization of previously glaciated areas mainly took place from the east of Europe. Despite the difference in life-history traits, the patterns found for the annual R. angustifolius show similarities with those of perennial species in terms of genetic diversity and geographic organization of genetic variation. Although organelle markers have typically been preferred in phylogeographic studies, the cpDNA variation in R. angustifolius did not show any clear geographic structure. The absence of geographic structure in the cpDNA variation may reflect persistence of ancestral polymorphisms or hybridization and introgression with closely-related species.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 1–13.     

Allozyme diversity and history of distribution expansion in the maritime perennial plant Hedyotis strigulosa (Rubiaceae), distributed over the wide latitudes in the Japanese Archipelago

Allozyme diversity was examined in 30 populations of the maritime perennial plant Hedyotis strigulosa var. parviflora , which is distributed from subtropical islands to the central mainland of Japan. Genetic diversity within populations tended to be larger in southern island populations than in northern mainland populations. In the southern part of the distribution, the population size is generally large and populations are distributed more continuously than in the northern area, resulting in the larger effective size of southern populations as a whole. These factors play a major role in maintaining greater genetic diversity in the southern populations. By contrast, genetic diversity in the northern populations is very low, probably resulting from bottlenecks of population establishments during recolonization from refugial area to the northern areas. Geographically close populations were located near each other in the multidimensional scaling and the phenogram based on genetic distances, suggesting that gene flow among remote populations is rather limited. The pattern of genetic diversity in H. strigulosa var. parviflora is likely caused by the distribution expansion of the species; in the last glacier era, the species was restricted to the southern area; its advance to the northern area is relatively recent. Another variety endemic only to the Daito Islands, H. strigulos a var. luxurians , has lower genetic diversity than H. strigulosa var. parviflora and has genetically diverged from H. strigulosa var. parviflor a.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 679–688.