Cytonuclear discordance in the crowned-sparrows, Zonotrichia atricapilla and Zonotrichia leucophrys: a mitochondrial selective sweep?

ABSTRACTThe golden-crowned (Zonotrichia atricapilla) and white-crowned (Z. leucophrys) sparrows have been presented as a compelling case for rapid speciation. They display divergence in song and plumage with overlap in their breeding ranges implying reproductive isolation, but have almost identical mitochondrial genomes. Previous research proposed hybridization and subsequent mitochondrial introgression as an alternate explanation, but lacked robust nuclear gene trees to distinguish between introgression and incomplete lineage sorting. We test for signatures of these processes between Z. atricapilla and Z. leucophrys, and investigate the relationships among Z. leucophrys subspecies, using mitochondrial sequencing and a reduced representation nuclear genomic dataset. Contrary to the paraphyly evident in mitochondrial gene trees, we confirmed the reciprocal monophyly of Z. atricapilla and Z. leucophrys using large panels of single nucleotide polymorphism (SNPs). The pattern of cytonuclear discordance is consistent with limited, historical hybridization and mitochondrial introgression, rather than a recent origin and incomplete lineage sorting between recent sister species. We found evidence of nuclear phylogeographic structure within Z. leucophrys with two distinct clades. Altogether, our results support the true species status of Z. atricapilla and Z. leucophrys, and indicate deeper divergences between the two species than inferred using mitochondrial markers. Our results demonstrate the limitations of relying solely on mitochondrial DNA for taxonomy, and raise questions about the possibility of selection on the mitochondrial genome during temperature oscillations (e.g. during the Pleistocene). Historical mitochondrial introgression facilitated by past environmental changes could cause erroneous dating of lineage splitting in other taxa when based on mitochondrial DNA alone.

Evidence of hybridization, mitochondrial introgression and biparental inheritance of the kDNA minicircles in Trypanosoma cruzi I

BackgroundGenetic Exchange in Trypanosoma cruzi is controversial not only in relation to its frequency but also in relation to its mechanism. A mechanism of parasexuality has been proposed based on laboratory hybrids, but population genomics strongly suggests meiosis. In addition, mitochondrial introgression has been reported several times in natural isolates although its mechanism is not clear. Moreover, hybrid DTUs (TcV and TcVI) have inherited at least part of the kinetoplastic DNA (kDNA = mitochondrial DNA) from both parents.Methodology/Principal findingsIn order to address such topics, we sequenced and analyzed fourteen nuclear DNA fragments and three kDNA maxicircle genes in three TcI stocks which are natural clones potentially involved in events of genetic exchange. We also deep-sequenced (a total of 6,146,686 paired-end reads) the hypervariable region of kDNA minicircles (mHVR) in such three strains. In addition, we analyzed the DNA content by flow cytometry to address cell ploidy. We observed that most polymorphic sites in nuclear loci showed a hybrid pattern in one cloned strain and the other two cloned strains were compatible as parental strains (or nearly related to the true parents). The three clones have almost the same ploidy and the DNA content was similar to the reference strain Sylvio (an almost diploid strain). Despite maxicircle genes evolve faster than nuclear housekeeping ones, we did not detect polymorphism in the sequence of three maxicircle genes showing mito-nuclear discordance. In addition, the hybrid stock shared 66% of its mHVR clusters with one putative parental and 47% with the another one. In contrast, the putative parental stocks shared less than 30% of the mHVR clusters among them.Conclusions/significanceThe results suggest a reductive division, a natural hybridization, biparental inheritance of the minicircles in the hybrid and maxicircle introgression. The models including such phenomena and that would explain the relationships between these three clones are discussed.Author summaryChagas disease, an important public health problem in Latin America, is caused by the parasite Trypanosoma cruzi. Despite it is a widely studied parasite, several questions about the biology of genetic exchange remain. Meiosis has not been yet observed in laboratory, although inferred from population genomic studies. In addition, previous results suggest that the mitochondrial DNA (called kDNA) may be inherited from both parents in hybrids. Here, we analyzed a hybrid strain and the potential parents to address about the mechanisms of genetic exchange at nuclear and mitochondrial level. We observed that the hybrid strain has heterozygous patterns and DNA content compatible with an event of meiosis. In addition, we observed that the evolutionary histories of nuclear DNA and maxicircles (a part of the kDNA) were discordant and the three strains share identical DNA sequences. Mitochondrial introgression of maxicircle DNA from one genotype to another may explain this observation. In addition, we detected that the hybrid strain shared minicircles (another part of the kDNA) with both parental strains. Our results suggest that hybridization implied meiosis and biparental inheritance of the kDNA. Further research is required to address such phenomena in detail.

Mitochondrial Introgression, Color Pattern Variation, and Severe Demographic Bottlenecks in Three Species of Malagasy Poison Frogs, Genus Mantella

Madagascar is a biodiversity hotspot particularly rich in amphibian diversity and only a few charismatic Malagasy amphibians have been investigated for their population-level differentiation. The Mantella madagascariensis group is composed of two rainforest and three swamp forest species of poison frogs. We first confirm the monophyly of this clade using DNA sequences of three nuclear and four mitochondrial genes, and subsequently investigate the population genetic differentiation and demography of the swamp forest species using one mitochondrial, two nuclear and a set of nine microsatellite markers. Our results confirm the occurrence of two main mitochondrial lineages, one dominated by Mantella aurantiaca (a grouping supported also by our microsatellite-based tree) and the other by Mantella crocea + Mantella milotympanum. These two main lineages probably reflect an older divergence in swamp Mantella. Widespread mitochondrial introgression suggests a fairly common occurrence of inter-lineage gene flow. However, nuclear admixture seems to play only a limited role in this group, and the analyses of the RAG-1 marker points to a predominant incomplete lineage sorting scenario between all five species of the group, which probably diverged relatively recently. Our demographic analyses show a common, severe and recent demographic contraction, inferred to be in temporal coincidence with the massive deforestation events that took place in the past 1000 years. Current data do not allow to conclusively delimit independent evolutionary units in these frogs, and we therefore refrain to suggest any taxonomic changes.