Distinguishing between Incomplete Lineage Sorting and Genomic Introgressions : Complete Fixation of Allospecific Mitochondrial DNA in a Sexually Reproducing Fish (Cobitis; Teleostei), despite Clonal Reproduction of Hybrids

Peer reviewe

Depleted genetic variation of the European ground squirrel in Central Europe in both microsatellites and the major histocompatibility complex gene: Implications for conservation

Habitat fragmentation may influence the genetic make-up and adaptability of endangered populations. To facilitate genetic monitoring of the endangered European ground squirrel (EGS), we analyzed 382 individuals from 16 populations in Central Europe, covering almost half of its natural range. We tested how fragmentation affects the genetic architecture of presumably selectively neutral (12 microsatellites) and non-neutral (the major histocompatibility class II DRB gene) loci. Spatial genetic analyses defined two groups of populations, "western" and "eastern", with a significantly higher level of habitat fragmentation in the former group. The highly fragmented western populations had significantly lower genetic diversity in both types of markers. Only one allele of the DRB gene predominated in populations of the western group, while four alleles were evenly distributed across the eastern populations. Coefficient of inbreeding values (FIS) calculated from microsatellites were significantly higher in the western (0. 27-0. 79) than in eastern populations (-0. 060-0. 119). Inter-population differentiation was very high, but similar in both groups (western FST = 0. 23, eastern FST = 0. 25). The test of isolation by distance was significant for the whole dataset, as well as for the two groups analyzed separately. Comparison of genetic variability and structure on microsatellites and the DRB gene does not provide any evidence for contemporary selection on MHC genes. We suggest that genetic drift in small bottlenecked and fragmented populations may overact the role of balancing selection. Based on the resulting risk of inbreeding depression in the western populations, we support population management by crossbreeding between the western and eastern populations. © 2011 Springer Science+Business Media B.V

Spined loaches (<i>Cobitis</i>) used in this study.

<p>Spined loaches (<i>Cobitis</i>) used in this study.</p

Prior and posterior distributions of parameters in the BPP Bayesian analysis of the nine nuclear loci.

a<p>Priors set with <i>Ne</i> = 225,000 covering Watterson's <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080641#pone.0080641-Watterson1" target="_blank">[91]</a> θ estimate (<i>θ</i>_W = 0.002, <i>Ne = </i>138,889) and from branching event t = 3.31 Mya between European closely related <i>Cobitis</i> species <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080641#pone.0080641-Tang1" target="_blank">[104]</a>. Relatively fast autosomal mutation rate (<i>μ</i>) of 3.6×10⁻⁹ estimated in vertebrates <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080641#pone.0080641-Axelsson1" target="_blank">[105]</a> was used to transform prior expectations of <i>θ</i> and <i>τ</i> from absolute estimates of <i>N_e</i> and t. Both <i>τ</i> and <i>θ</i> are measured as the expected number of mutations per site.</p>b<p>Prior for the node age was generated from the Dirichlet distribution (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080641#pone.0080641-Yang1" target="_blank">[63]</a>: equation 2).</p><p><i>C. tae</i> = <i>C. taenia</i>, <i>C. tan</i> = <i>C. tanaitica</i>, <i>C. elo</i> = <i>C. elongatoides.</i></p

Probability densities of four parameters in coalescence simulation as functions of length of internode.

<p>Graphical visualization in which (1–P_{Concord-mtDNA}) denotes the probability density of observing discordant mtDNA phylo tree; (P_binom-nuc) denotes the probability density of observing eight topologically concordant nuclear gene trees out nine studied nuclear loci in total; (P_Coal-mtDNA) denotes the cumulative probability of mtDNA coalescence along the internode and (P_Coal-nuc) denotes the cumulative probability of coalescence of nuclear locus along the internode. Note that there is very small intersection of probability densities allowing for observing eight out of nine topologically concordant nuclear loci while having discordant mtDNA tree (see the text for details).</p

Photographs, karyotypes and Europe-wide distribution of spined loach sexual species (<i>Cobitis</i>) from this study.

<p>(A,C,E) Photographs (scale bar = 1 cm) and (B,D,F) respective karyotypes of three widespread <i>Cobitis</i> species. Karyograms with diploid chromosome number (2n), metacentric (m), submetacentric (sm), subtelocentric (st), and acrocentric chromosomes (a) were modified after Janko et al. <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080641#pone.0080641-Janko2" target="_blank">[50]</a>; (G) Sampling localities of <i>Cobitis taenia</i> (light gray squares; 1–10), <i>C. elongatoides</i> (dark gray squares; 11–20), <i>C. tanaitica</i> (black squares; 21–30), <i>C. paludica</i> (checkered square; 31), <i>C. fahirae</i> (spotted square; 32), and <i>C. vardarensis</i> (reticulated square; 33). Insets show European species distribution with respective markings as given in squares. Note that locality no. 1 is situated more eastward, as marked by the arrow.</p

Posterior probability distributions for migration rates from two-population IM analysis.

<p>Coalescent-based estimates of migration rates (scaled by mutation rate) for three studied species inferred separately from (A–C) nuclear sequence data that included nine nuclear markers, and from (D–H) one mitochondrial marker gene.</p

Phylogenetic comparison of gene trees constructed from nuclear and mitochondrial gene markers and mito-nuclear discordance.

<p>Bayesian DNA gene trees constructed from nine nuclear gene markers and one mitochondrial <i>cytb</i> gene marker were rooted with sequences from <i>C. paludica</i>. Haplotype numbers correspond to <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080641#pone-0080641-t002" target="_blank">Table 2</a>. Bar represents 0.1 substitution/site. The schematic tree shows the phylogenetic conflict of <i>C. tanaitica</i> topology between mitochondrial and nuclear gene markers.</p

Parameters calculated from alternative tests using sequence data to explain <i>C. tanaitica</i> mito-nuclear discordance.

<p>Contemporary and ancestral population sizes are denoted by (<i>θ_C.tae</i>, <i>θ_C.tan</i>_,<i>θ_C.elo</i>_,<i>θ_C.tae,C.tan</i>, <i>θ_{C.tae,C.tan,C.elo}</i>). Divergence times are denoted by (<i>τ_C.tae,C.tan</i> and <i>τ_{C.tae,C.tan,C.elo}</i>), and interval between those times is denoted by (<i>γ</i>). Migration rates are denoted by (<i>m</i>) with relevant index. All parameters are scaled by mutation rate <i>μ</i>, and can be converted to absolute values using the relations <i>θ</i> = 4<i>Nμ</i> (where <i>N</i> is effective population size), <i>m</i> = m/<i>μ</i> (where m is gene-flow rates per gene copy per generation, <i>τ</i> = t<i>μ</i> (where t is a time of population splitting at <i>τ</i> generations in the past), and <i>γ</i> = t<i>μ</i>. Parameters estimated by BPP program are denoted by ($), those by IM by (#), and those by IMa2 by (@). The parameter <i>γ</i> was calculated from <i>τ</i>s given by BPP and ds programmes. <i>C. taenia</i> (<i>C.tae</i>), <i>C. tanaitica</i> (<i>C. tan</i>), and <i>C. elongatoides</i> (<i>C. elo</i>).</p