Manuel Ruedi

THE HIDDEN SIDE OF INVASIONS: MASSIVE INTROGRESSION BY LOCAL GENES

Abstract Despite hundreds of reports involving both plants and animals, the mechanisms underlying introgression remain obscure, even if some form of selection is frequently invoked. Introgression has repeatedly been reported in species that have recently colonized a new habitat, suggesting that demographic processes should be given more attention for understanding the mechanisms of introgression. Here we show by spatially explicit simulations that massive introgression of neutral genes takes place during the invasion of an occupied territory if interbreeding is not severely prevented between the invading and the local species. We also demonstrate that introgression occurs almost exclusively from the local to the invading species, especially for populations located far away from the source of the invasion, and this irrespective of the relative densities of the two species. This pattern is strongest at markers experiencing reduced gene flow, in keeping with the observation that organelle genes are often preferentially introgressed across species boundaries. A survey of the literature shows that a majority of published empirical studies of introgression during range expansions, in animals and in plants, follow the predictions of our model. Our results imply that speciation genes can be identified by comparing genomes of interfertile native and invading species pairs.

Segmental copy number variation shapes tissue transcriptomes

Copy number variation (CNV) is a key source of genetic diversity, but a comprehensive understanding of its phenotypic effect is only beginning to emerge. We have generated a CNV map in wild mice and classical inbred strains. Genome-wide expression data from six major organs show not only that expression of genes within CNVs tend to correlate with copy number changes, but also that CNVs influence the expression of genes in their vicinity, an effect that extends up to half a megabase. Genes within CNVs show lower expression and more specific spatial expression patterns than genes mapping elsewhere. Our analyses reveal differential constraint on copy number changes of genes expressed in different tissues. Dosage alterations of brain-expressed genes are less frequent than those of other genes and are buffered by tighter transcriptional regulation. Our study provides initial evidence that CNVs shape tissue transcriptomes on a global scale.

Is the Gibraltar Strait a barrier to gene flow for the bat Myotis myotis (Chiroptera: Vespertilionidae)?

Because of their role in limiting gene flow, geographical barriers like mountains or seas often coincide with intraspecific genetic discontinuities. Although the Strait of Gibraltar represents such a potential barrier for both plants and animals, few studies have been conducted on its impact on gene flow. Here we test this effect on a bat species (Myotis myotis) which is apparently distributed on both sides of the strait. Six colonies of 20 Myotis myotis each were sampled in southern Spain and northern Morocco along a linear transect of 1350 km. Results based on six nuclear microsatellite loci reveal no significant population structure within regions, but a complete isolation between bats sampled on each side of the strait. Variability at 600 bp of a mitochondrial gene (cytochrome b) confirms the existence of two genetically distinct and perfectly segregating clades, which diverged several million years ago. Despite the narrowness of the Gibraltar Strait (14 km), these molecular data suggest that neither males, nor females from either region have ever reproduced on the opposite side of the strait. Comparisons of molecular divergence with bats from a closely related species (M. blythii) suggest that the North African clade is possibly a distinct taxon warranting full species rank. We provisionally refer to it as Myotis cf punicus Felten 1977, but a definitive systematic understanding of the whole Mouse‐eared bat species complex awaits further genetic sampling, especially in the Eastern Mediterranean areas.

Contrasted patterns of mitochondrial and nuclear structure among nursery colonies of the bat Myotis myotis

Thirteen nursery colonies of Myotis myotis were sampled in central Europe to investigate the dispersal behaviour of this bat species. Mitochondrial DNA sequences of 260 bats reveal the occurrence of three evolutionary lineages that have probably originated in distinct glacial refugia and meet in a contact zone near the Alps. Moreover, the strong haplotypic segregation (ΦST=0.540) suggests that breeding females are philopatric. Contrastingly, the low population structure at 15 microsatellite loci (FST=0.022), suggests the homogenizing effect of nuclear gene flow. The different perspectives given by these two markers are consistent with strong male‐biased dispersal. As a result of female philopatry, the local haplotypic variability seems to be largely influenced by historical processes of colonization. Conversely, the homogeneity of nuclear variability within roosts that are located north of the Alps seems to mainly reflect contemporary gene flow. Finally, despite the fact that females are faithful to their natal colony, movements of both males and females occur outside the breeding period. Mitochondrial survey of individuals sampled exclusively in nurseries may thus poorly reflect the metapopulation dynamics of this species.

Recurrent replacement of mtDNA and cryptic hybridization between two sibling bat species Myotis myotis and Myotis blythii

The two sibling bat species Myotis myotis and Myotis blythii occur in sympatry over wide areas of Southern and Central Europe. Morphological, ecological and previous genetic evidences supported the view that the two species constitute two well-differentiated groups, but recent phylogenetic analyses have shown that the two species shared some mtDNA haplotypes when they occurred in sympatry. In order to see whether some genetic exchange occurred between the two species, we sequenced a highly variable segment of the mitochondrial control region in both species living in sympatry and in allopatry. We also analysed the nuclear diversity of 160 individuals of both species found in two mixed nursery colonies located north and south of the Alps. MtDNA analysis confirmed that European M. blythii share multiple, identical or very similar haplotypes with M. myotis. Since allopatric Asian M. blythii presents mtDNA sequences that are very divergent from those of the two species found in Europe, we postulate that the mitochondrial genome of the European M. blythii has been replaced by that of M. myotis. The analysis of nuclear diversity shows a strikingly different pattern, as both species are well differentiated within mixed nursery colonies (FST=0.18). However, a Bayesian analysis of admixture reveals that the hybrids can be frequently observed, as about 25% of sampled M. blythii show introgressed genes of M. myotis origin. Contrastingly, less than 4% of the M. myotis analysed were classified as non-parental genotypes, revealing an asymmetry in the pattern of hybridization between the two species. These results show that the two species can interbreed and that the hybridization is still ongoing in the areas of sympatry. The persistence of well-differentiated nuclear gene pools, in spite of an apparent replacement of mitochondrial genome in European M. blythii by that of M. myotis, is best explained by a series of introgression events having occurred repeatedly during the recent colonization of Europe by M. blythii from Asia. The sharp contrast obtained from the analysis of mitochondrial and nuclear markers further points to the need to cautiously interpret results based on a single class of genetic markers.

The Iberian contribution to cryptic diversity in European bats

ABSTRACT We investigate the contribution of the Iberian bat fauna to the cryptic diversity in Europe using mitochondrial (cytb and ND1) and nuclear (RAG2) DNA sequences. For each of the 28 bat species known for Iberia, samples covering a wide geographic range within Spain were compared to samples from the rest of Europe. In this general screening, almost 20% of the Iberian species showed important mitochondrial discontinuities (K2P distance values > 5%) either within the Iberian or between Iberian and other European samples. Within Eptesicus serotinus and Myotis nattereri, levels of genetic divergence between lineages exceeded 16%, indicating that these taxa represent a complex of several biological species. Other well-differentiated lineages (K2P distances between 5–10%) appeared within Hypsugo savii, Pipistrellus kuhlii and Plecotus auritus, suggesting the existence of further cryptic diversity. Most unsuspected lineages seem restricted to Iberia, although two have crossed the Pyrenees to reach, at least, Switzerland.

Phylogeny of African Myotis Bats (Chiroptera, Vespertilionidae) Inferred from Cytochrome b Sequences

The genus Myotis is comprised of about 100 species that are unequally distributed between the Northern (81% of the species) and the Southern hemisphere (19% of the species). Only eight species of Myotis occur in the Ethiopian region, but this is the only biogeographic region with representatives of all four classical subgenera, suggesting a diverse assemblage of morphotypes. We used sequences of a mitochondrial DNA gene (cyt b) to investigate the evolution and the phylogenetic position of seven of the eight Ethiopian species, and compared them to a broad sampling of Myotis from the World and of other vespertilionids. Phylogenetic reconstruction was based on 91 complete sequences representing 79 species of bats. The two endemic southern African species of the subgenus Cistugo were not placed within the genus Myotis, but were basal to the vespertilionid radiation, as suggested by earlier work based on karyology. The remaining Ethiopian species formed a strong monophyletic clade within Myotis, further stressing the importance of biogeography as a good predictor of phylogenetic relationships. This Ethiopian clade includes one Western Palaearctic and one Oriental species, both of which probably secondarily colonized these areas from the Ethiopian region. Molecular dating based on Bayesian inferences suggest that these faunal exchanges occurred at the end of the Miocene, while the split of the Ethiopian clade from the other Old World Myotis dates back to the middle Miocene, quite early in the Myotis radiation. Thus, the relative paucity of species in sub-Saharan Africa cannot be attributed to a late entry into this continent. Instead, these molecular results suggest that other evolutionary processes are responsible for the poor species diversity of Myotis found in Africa today.

Genetic consequences of the ice ages on nurseries of the bat Myotis myotis: a mitochondrial and nuclear survey

Analyses of mitochondrial DNA (mtDNA) control region polymorphism and of variation at 10 nuclear microsatellite loci were used to investigate the mechanisms and genetic consequences of postglacial expansion of Myotis myotis in Europe. Initial sampling consisted of 480 bats genotyped in 24 nursery colonies arranged along a transect of ≈ 3000 km. The phylogeographical survey based on mtDNA sequences revealed the existence of major genetic subdivisions across this area, with several suture zones between haplogroups. Such zones of secondary contact were found in the Alps and Rhodopes, whereas other potential barriers to gene flow, like the Pyrenees, did not coincide with genetic discontinuities. Areas of population admixture increased locally the genetic diversity of colonies, which confounded the northward decrease in nucleotide diversity predicted using classical models of postglacial range expansion. However, when analyses were restricted to a subset of 15 nurseries originating from a single presumed glacial refugium, mtDNA polymorphism did indeed support a northwards decrease in diversity. Populations were also highly structured (ΦST = 0.384). Conversely, the same subset of colonies showed no significant latitudinal decrease in microsatellite diversity and much less population structure (FST = 0.010), but pairwise genetic differentiation at these nuclear markers was strongly correlated with increasing geographical distance. Together, this evidence suggests that alleles carried via male bats have maintained enough nuclear gene flow to counteract the effects of recurrent bottlenecks generally associated with recolonization processes. As females are highly philopatric, we argue that the maternally transmitted mtDNA marker better reflects the situation of past, historical gene flow, whereas current levels of gene flow are better reflected by microsatellite markers.

Phylogenetic evidence of mitochondrial DNA introgression among pocket gophers in New Mexico (family Geomyidae)

Mitochondrial DNA (mtDNA) variation in the cytochrome b gene was determined for two divergent taxa of pocket gophers, Thomomys bottae actuosus and T. b. ruidosae. These two taxa hybridize in a narrow contact zone, but introgression of nuclear markers such as allozymes or chromosomes does not extend much beyond the hybrid zone (Patton et al. 1979). We found that despite their distinctness, the two subspecies shared very similar mtDNA haplotypes. By a comparison of phylogenetic histories derived from nuclear markers (allozymes) and from mtDNA haplotypes sampled in different populations of T. bottae from New Mexico, we show that apparent similarity is due to an introgression of T. b. ruidosae mtDNA into T. b. actuosus nuclear background. Evidence of introgression is not limited to the present‐day contact zone between these two taxa, but extends at least 75 km away from it. The actuosus haplotype coexists along with the ruidosae mtDNA in the Gallinas Mts., which are inhabited by otherwise pure T. b. actuosus, while further north only typical actuosus haplotypes were detected. Of several potential mechanisms which could lead to such a geographical pattern of variation, we argue that a combination of range shifts due to climatic fluctuations, and genetic drift are most likely. Horizontal gene transfers due to hybridization are historical events which seem rather common among pocket gophers. Although they can be identified with careful phylogenetic study using independent data sets, the potential for misinterpreting a gene tree as an organismal tree is great in this and other groups of animals.

Molecular phylogenetics of Myotis indicate familial-level divergence for the genus Cistugo (Chiroptera)

Abstract The genus Myotis has undergone significant taxonomic revision since the advent of DNA sequencing techniques. Prior morphological examination of Myotis has indicated as many as 4 subgenera correlated with foraging strategies. Recent studies using mitochondrial DNA (mtDNA) sequence data have questioned the validity of these subgenera and have indicated that several taxa may require reevaluation as to their position within Vespertilionidae. Nevertheless, no study has used large-scale nuclear DNA sequencing to examine relationships within Myotis. We generated 4,656 base pairs (bp) of nuclear intron (PRKC1, STAT5A, and THY) and exon (APOB, DMP1, and RAG2) sequence data in addition to 2,866 bp of mtDNA sequence data to test previously hypothesized subgeneric groupings of Myotis. We included 21 species of Myotis from all morphological subgenera previously suggested, representatives of all subfamilies and tribes currently recognized in Vespertilionidae, and multiple representatives of all other families currently included in the superfamily Vespertilionoidea. We also included a representative of the rare African genus Cistugo, because significant doubt exists about its familial position. Our phylogenetic analyses did not support the morphologically defined Myotis subgenera and confirm that morphological similarities among Myotis are the result of convergent evolution. Divergence estimates derived from the total data set were concordant with previous studies, suggesting a middle Miocene trans-Beringian dispersal from Asia colonized North America, with subsequent South American colonization and diversification prior to the formation of the Isthmus of Panama 3–4 million years ago. Myotis latirostris fell outside of Myotis, and the high genetic distance separating it from other Myotis suggested that M. latirostris represented a distinct genus. The genus Cistugo, previously a subgenus within Myotis, fell basal to all vespertilionids, with a high genetic distance separating it from Vespertilionidae. We conclude that Cistugo should constitute a distinct family within Vespertilionoidea.