The biogeography of mitochondrial and nuclear discordance in animals

Combining nuclear (nuDNA) and mitochondrial DNA (mtDNA) markers has improved the power of molecular data to test phylogenetic and phylogeographic hypotheses and has highlighted the limitations of studies using only mtDNA markers. In fact, in the past decade, many conflicting geographic patterns between mitochondrial and nuclear genetic markers have been identified (i.e. mito-nuclear discordance). Our goals in this synthesis are to: (i) review known cases of mito-nuclear discordance in animal systems, (ii) to summarize the biogeographic patterns in each instance and (iii) to identify common drivers of discordance in various groups. In total, we identified 126 cases in animal systems with strong evidence of discordance between the biogeographic patterns obtained from mitochondrial DNA and those observed in the nuclear genome. In most cases, these patterns are attributed to adaptive introgression of mtDNA, demographic disparities and sex-biased asymmetries, with some studies also implicating hybrid zone movement, human introductions and Wolbachia infection in insects. We also discuss situations where divergent mtDNA clades seem to have arisen in the absence of geographic isolation. For those cases where foreign mtDNA haplotypes are found deep within the range of a second taxon, data suggest that those mtDNA haplotypes are more likely to be at a high frequency and are commonly driven by sex-biased asymmetries and/or adaptive introgression. In addition, we discuss the problems with inferring the processes causing discordance from biogeographic patterns that are common in many studies. In many cases, authors presented more than one explanation for discordant patterns in a given system, which indicates that likely more data are required. Ideally, to resolve this issue, we see important future work shifting focus from documenting the prevalence of mito-nuclear discordance towards testing hypotheses regarding the drivers of discordance. Indeed, there is great potential for certain cases of mitochondrial introgression to become important natural systems within which to test the effect of different mitochondrial genotypes on whole-animal phenotypes.     

Sympatric bromeliad species (Pitcairnia spp.) facilitate tests of mechanisms involved in species cohesion and reproductive isolation in Neotropical inselbergs

The roles of intra- and interspecific gene flow in speciation and species evolution are topics of great current interest in molecular ecology and evolutionary biology. Recent modelling studies call for new empirical data to test hypotheses arising from the recent shift from a 'whole-genome reproductive isolation' view to a 'genic' view of species and speciation. Particularly scarce (and thus of particular interest) are molecular genetic data on recently radiated, naturally hybridizing species in strongly structured and species-rich environments. Here, we studied four sympatric plant species (Pitcairnia spp.; Bromeliaceae) adapted to Neotropical inselbergs (isolated outcrops resembling habitat 'islands' in tropical rainforests) using nuclear and plastid DNA. Patterns of plastid DNA haplotype sharing and nuclear genomic admixture suggest the presence of both, incomplete lineage sorting and interspecific gene flow over extended periods of time. Integrity and cohesion of inselberg species of Pitcairnia are maintained despite introgression and in the face of extremely low within-species migration rates (N(e)m < 1 migrant per generation). Cross-evaluation of our genetic data against published pollination experiments indicate that species integrity is maintained by the simultaneous action of multiple prezygotic barriers, including flowering phenology, pollinator isolation and divergent mating systems. Postzygotic Bateson-Dobzhansky-Muller incompatibilities appear to contribute to isolation, as suggested by asymmetric introgression rates of single loci. Our results suggest that incomplete lineage sorting, hybridization and introgression form integral aspects of adaptive radiation in Neotropical inselberg 'archipelagos'. Inselbergs with multiple closely related co-occurring species should be of special interest to students of speciation in mountain systems, and to ongoing conservation programmes in the Atlantic Rainforest biodiversity hotspot.     

杯萼海桑和格氏海桑自然杂交的分子证据

Interspecific hybridization has been frequently observed in the mangrove genus Sonneratia. However, no natural hybridization has been reported between Sonneratia alba and S. griffithii to date, despite their overlapping distribution in the coast of Andaman Sea. In this study, cysteine proteinase inhibitor gene (cpi) from the nuclear genome, and two intergenic spacers (trnL-trnF and trnV-trnM) from the chloroplast genome, were sequenced to determine whether natural hybridization took place between the two species. Our results revealed two distinct types of cpi sequences from the putative hybrid matching those acquired from S. griffithii and S. alba, respectively. Sequencing of the chloroplast trnL-trnF and trnV-trnM regions showed that S. alba differed from S. griffithii by one nucleotide in each region, and the putative hybrid had the identical sequences with S. griffithii. Molecular data demonstrated clearly that there indeed existed natural hybridization between S. alba and S. griffithii, and that S. griffithii was the maternal parent in this hybridization event.     

Hybridization between ecotypes in a phenotypically and ecologically heterogeneous population of Iris savannarum (Iridaceae) in Florida

Iris series Hexagonae is a small, monophyletic complex of five species and associated hybrid populations, popularly known as the ‘Louisiana irises’. Series Hexagonae has been recognized as a textbook case of introgressive hybridization based on numerous studies in Louisiana. We previously explored patterns of genetic structure and diversity in populations of the complex in Florida. Populations that occupy high, dry habitats have plants with a distinctive floral ‘highlands’ phenotype. Aquatic populations of I. savannarum also have a consistent floral phenotype (‘coastal’). Jacks Branch slough in Glades County harbors the largest population of series Hexagonae sampled in our previous studies. It is an ecologically heterogeneous site, punctuated by sandy uplands that remain above high water and harbor Iris with the highlands floral phenotype as well as coastal types in the wetter areas of the slough. We hypothesized that mesic, but non‐inundated, sites in the slough would host hybrids of the two phenotypic groups, and tested these hypotheses with 19 microsatellite loci. All data analyses support our hypothesis of hybridization between the upland and hydric subpopulations. Although two methods of introgression analysis identify some of the individuals from the admixture zone as first‐generation hybrids, subsequent admixture was asymmetric with introgression from the ‘highland’ parent. This is the first report of such assortative processes occurring in the confines of a single population of Iris. We suggest that the evolutionary processes described interspecifically for series Hexagonae commence early at the population level.     

Reticulate evolution of the Daphnia pulex complex as revealed by nuclear markers

The study of species complexes is of particular interest to understand how evolutionary young species maintain genomic integrity. The Daphnia pulex complex has been intensively studied as it includes species that dominate freshwater environments in the Northern hemisphere and as it is the sole North American complex that shows transitions to obligate parthenogenesis. Past studies using mitochondrial markers have revealed the presence of 10 distinct lineages in the complex. This study is the first to examine genetic relationships among seven species of the complex at nuclear markers (nine microsatellite loci and one protein-coding gene). Clones belonging to the seven species of the Daphnia pulex complex were characterized at the mitochondrial NADH dehydrogenase (ND5) gene and at the Lactate dehydrogenase (LDH) locus. K-means, principal coordinate analyses and phylogenetic network analyses on the microsatellite data all separated European D. pulicaria, D. tenebrosa, North American D. pulex, D. pulicaria and their hybrids into distinct clusters. The hybrid cluster was composed of diploid and polyploid hybrids with D. pulex mitochondria and some clones with D. pulicaria mitochondria. By contrast, the phylogeny of the D. pulex complex using Rab4 was not well resolved but still showed clusters consisting mostly of D. pulex alleles and others of D. pulicaria alleles. Incomplete lineage sorting and hybridization may obscure genetic relationships at this locus. This study shows that hybridization and introgression have played an important role in the evolution of this complex.     

Somatic hybrids between potato <Emphasis Type="Italic">Solanum tuberosum</Emphasis> and wild species <Emphasis Type="Italic">Solanum verneï</Emphasis> exhibit a recombination in the plastome

In the present survey, interspecific somatic protoplast fusion between a dihaploid cultivated potato Solanum L. tuberosum (BF15) and a wild species Solanum verneï (V3) has been performed using the PEG method. Five putative hybrids were first selected. Among them, only two were retained. DNA analysis, using flow cytometry, showed that the first hybrid (VB2) was dihaploid (2n=2x=24 chromosomes), whereas the second (VB1) was hexaploid (2n=6x=72 chromosomes). In the greenhouse, these putative hybrids showed that they were able of raising and producing large tubers but with a modified shape compared to parental ones. Furthermore, they harbored an intermediate leaf morphology compared to their parents. The hybrid nature of these plants was first confirmed according to their esterase and peroxidase isoenzyme patterns. The RAPD analysis of genomic DNA and microsatellite based amplification (I-SSR) showed that both clones VB1 and VB2 are asymmetric somatic hybrids. They seem to have eliminated the major part of V3 parental nucleus but not the totality. The analysis of chloroplast DNA suggests that both hybrid plastomes were the result of a recombination between parental ones.     

植物叶绿体4.5S核糖体rRNA作为分子杂交探针的研究

我们提取纯化了芹菜,菠菜和蕃茄叶绿体核糖体4.5SRNA(4.5SrRNA)并在其5’端标记~(32)P,作为探针与菠菜,蕃茄和芹菜叶绿体DNA(ctDNA)进行分子杂交。结果不仅证明4.5SrRNA可作为公用分子杂交探针,而且也说明不同植物4.5SrRNA序列有相当大的同源性。     

Speciation via introgressive hybridization in East African cichlids?

Speciation caused by introgressive hybridization occurs frequently in plants but its importance remains controversial in animal evolution. Here we report a case of introgressive hybridization between two ancient and genetically distinct species of Lake Tanganyika cichlids that led to the formation of a new species. Neolamprologus marunguensis contains mtDNA haplotypes from both parental species varying on average by 12.4% in the first section of the control region and by 5.2% in a segment of the cytochrome b gene. All individuals have almost identical DNA sequences in the flanking regions of the single-copy nuclear DNA locus TmoM27, and show a mosaic of alleles derived from both parental lineages in six microsatellite loci. Hence, our finding displays another mode of speciation in cichlid fishes. The increase of genetic and phenotypic diversity due to hybridization may contribute to the uniquely rapid pace of speciation in cichlids.     

Nonuniform concerted evolution and chloroplast capture: heterogeneity of observed introgression patterns in three molecular data partition phylogenies of Asian Mitella (saxifragaceae)

Interspecific hybridization is one of the major factors leading to phylogenetic incongruence among loci, but the knowledge is still limited about the potential of each locus to introgress between species. By directly sequencing three DNA regions: chloroplast DNAs (matK gene and trnL-F noncoding region), the nuclear ribosomal external transcribed spacer (ETS) region, and internal transcribed spacer (ITS) regions, we construct three phylogenetic trees of Asian species of Mitella (Saxifragaceae), a genus of perennials in which natural hybrids are commonly observed. Within this genus, there is a significant topological conflict between chloroplast and nuclear phylogenies and also between the ETS and the ITS, which can be attributed to frequent hybridization within the lineage. Chloroplast DNAs show the most extensive introgression pattern, ITS regions show a moderate pattern, and the ETS region shows no evidence of introgression. Nonuniform concerted evolution best explains the difference in the introgression patterns between the ETS region and ITS regions, as the sequence heterogeneity of the ITS region within an individual genome is estimated to be twice that of an ETS in this lineage. Significant gene conversion patterns between two hybridizing taxa were observed in contiguous arrays of cloned ETS-ITS sequences, further confirming that only ITS regions have introgressed bidirectionally. The relatively slow concerted evolution in the ITS regions probably allows the coexistence of multiple alleles within a genome, whereas the strong concerted evolution in the ETS region rapidly eliminates heterogeneous alleles derived from other species, resulting in species delimitations highly concordant with those based on morphology. This finding indicates that the use of multiple molecular tools has the potential to reveal detailed organismal evolution processes involving interspecific hybridization, as an individual locus varies greatly in its potential to introgress between species.     

小麦与高冰草体细胞杂种后代的核基因组和叶绿体基因组的遗传特征

以小麦(TriticumaestivumL.)与高冰草(Agropyronelongatum(Host)Nevski)体细胞杂种同一个克隆来源的F2-F6自交系Ⅱ-2、Ⅱ-Ⅰ-8以及由Ⅱ-Ⅰ-8F2分离形成的8-1(F3-F6)为材料,利用小麦叶绿体基因组的微卫星(Microsatellite)特异引物及随机扩增多态性DNA(RAPD)引物进行分析。结果表明,杂种株系的叶绿体基因组组成一致,均以小麦叶绿体基因组为主,仅在rpl14和rpl16基因的间隔序列中检测到双亲的特征带,表明有高冰草的叶绿体DNA在杂种中存在,并稳定遗传至第六代。RAPD分析表明,不同杂种株系中存在不同的高冰草核DNA片段,核基因组在传代中基本稳定。