Integrative taxonomic revision of the New Caledonian endemic genus Taophila Heller (Coleoptera: Chrysomelidae, Eumolpinae)

There are 96 endemic species of Eumolpinae (Coleoptera: Chrysomelidae) described from New Caledonia, but some estimates propose that the actual number could be at least twice this figure. Not surprisingly, when a particular species assemblage has been revised, the number of species in that group increases significantly. Here, we revise the New Caledonian endemic genus Taophila Heller, 1916, the best studied in this fauna and currently known to include eleven species, one in the subgenus Jolivetiana Gómez-Zurita & Cardoso, 2014, and ten in the nominal subgenus. The analysis of morphological differences in a large sample of Taophila and the validation of the resulting species hypotheses in an integrative fashion based on a phylogenetic analysis of partial mtDNA sequences (cox1 and rrnS) resulted in the addition of eleven more taxa. Taxonomic splits mainly reinterpreted the previous observation of mtDNA paraphyly affecting T. subsericea Heller, 1916, shown to represent a complex of species mostly distinguishable by diagnostic differences among females. The new species described are: T. bituberculata n. sp., T. carinata n. sp., T. dapportoi n. sp., T. davincii n. sp., T. draco n. sp., T. goa n. sp., T. hackae n. sp., T. samuelsoni n. sp., T. sideralis n. sp., T. taaluny n. sp. and T. wanati n. sp. These additions and the synonymy T. subsericea Heller = Stethotes mandjeliae Jolivet, Verma & Mille, 2010 n. syn., bring to 21 the total number of species in Taophila. Moreover, we also found the first evidence of mtDNA introgression between species of New Caledonian Eumolpinae, resulting from putative recent hybridization of T. subsericea and T. dapportoi where these species coexist. We describe a model incorporating the mtDNA genealogy of T. subsericea about the conditions that may have favored the secondary geographic encounter required for the hybridization of these species.

The unidirectional phylogeny of Homo sapiens anchors the origin of modern humans in Eurasia

Background The Out of Africa hypothesis, OOAH, was challenged recently in an extended mtDNA analysis, PPA (Progressive Phylogenetic Analysis), that identified the African human populations as paraphyletic, a finding that contradicted the common OOAH understanding that Hss had originated in Africa and invaded Eurasia from there. The results were consistent with the molecular Out of Eurasia hypothesis, OOEH, and Eurasian palaeontology, a subject that has been largely disregarded in the discussion of OOAH. Results In the present study the mtDNA tree, a phylogeny based on maternal inheritance, was compared to the nuclear DNA tree of the paternally transmitted Y-chromosome haplotypes, Y-DNAs. The comparison showed full phylogenetic coherence between these two separate sets of data. The results were consistent with potentially four translocations of modern humans from Eurasia into Africa, the earliest taking place ≈ 250,000 years before present, YBP. The results were in accordance with the postulates behind OOEH at the same time as they lent no support to the OOAH. Conclusions The conformity between the mtDNA and Y-DNA phylogenies of Hss is consistent with the understanding that Eurasia was the donor and not the receiver in human evolution. The evolutionary problems related to OOAH became similarly exposed by the mtDNA introgression that took place from Hss into Neanderthals ≈ 500,000 YBP, a circumstance that demonstrated the early coexistence of the two lineages in Eurasia.

Mitonuclear co-introgression opposes genetic differentiation between phenotypically divergent songbirds

Comparisons of genomic variation among closely related species often show more differentiation in mitochondrial DNA (mtDNA) and sex chromosomes than in autosomes, a pattern expected due to the relative effective population sizes of these genomic components. Differential introgression can cause some species pairs to deviate dramatically from this pattern. The yellowhammer (Emberiza citrinella) and the pine bunting (E. leucocephalos) are hybridizing avian sister species that differ greatly in appearance but show no mtDNA differentiation. This discordance might be explained by mtDNA introgression-a process that can select for co-introgression at nuclear genes with mitochondrial functions (mitonuclear genes). We investigated genome-wide nuclear differentiation between yellowhammers and pine buntings and compared it to what was seen previously in the mitochondrial genome. We found clear nuclear differentiation that was highly heterogeneous across the genome, with a particularly wide differentiation peak on the sex chromosome Z. We further tested for preferential introgression of mitonuclear genes and detected evidence for such biased introgression in yellowhammers. Mitonuclear co-introgression can remove post-zygotic incompatibilities between species and may contribute to the continued hybridization between yellowhammers and pine buntings despite their clear morphological and genetic differences. As such, our results highlight the potential ramifications of co-introgression in species evolution.

Species limits in birds: Australian perspectives on interrelated challenges of allopatry, introgression of mitochondrial DNA, recent speciation, and selection

Four main challenges that can underpin ongoing, intransigent debates about species limits in birds are reviewed: allopatry (population subdivision vs. speciation), geographically widespread introgression of mitochondrial DNA (mtDNA), recent speciation, and selection. Examples from birds of the Australian region show how these challenges, their interplay, and the molecular-phenotypic discordance they generate can clarify or mislead species limits. Examples of how phylogenetic frameworks help reject or retain hypotheses of species limits under these challenges are given. Although mtDNA’s strengths and limitations are well known, an underappreciated limitation of mtDNA is geographically widespread introgression that homogenizes mtDNA diversity across species, subspecies, or population boundaries and across hundreds of kilometers. The resulting discordance between mtDNA and phenotype can be profound. If undetected, the setting of species limits and evolutionarily significant units are misled. An example shows how recent genomic analyses can detect and solve the problem. Other examples concern legacy mtDNA-only datasets. These are often essentially unfinished studies leaving residual uncertainty in species limits. Examples illustrate when the possibility of large-scale introgression across species boundaries needs to be considered, and how genomic scale data offer solutions. Researchers must carefully parse 3 questions: has there been introgression of mtDNA and, if so, which population genetics-based driver has caused introgression, and do species limits need altering? Understanding of allopatry, mtDNA introgression, recent speciation, and selection must be properly integrated if species limits are to be robustly understood and applied with maximum benefit in downstream applications such as conservation and management.

Comparative mitogenome analyses uncover mitogenome features and phylogenetic implications of the subfamily Cobitinae

Background Loaches of Cobitinae, widely distributed in Eurasian continent, have high economic, ornamental and scientific value. However, the phylogeny of Cobitinae fishes within genera or family level remains complex and controversial. Up to now, about 60 Cobitinae mitogenomes had been deposited in GenBank, but their integrated characteristics were not elaborated. Results In this study, we sequenced and analyzed the complete mitogenomes of a female Cobits macrostigma. Then we conducted a comparative mitogenome analysis and revealed the conserved and unique characteristics of 58 Cobitinae mitogenomes, including C. macrostigma. Cobitinae mitogenomes display highly conserved tRNA secondary structure, overlaps and non-coding intergenic spacers. In addition, distinct base compositions were observed among different genus and significantly negative linear correlation between AT% and AT-skew were found among Cobitinae, genus Cobitis and Pangio mitogenomes, respectively. A specific 3 bp insertion (GCA) in the atp8-atp6 overlap was identified as a unique feature of loaches, compared to other Cypriniformes fish. Additionally, all protein coding genes underwent a strong purifying selection. Phylogenetic analysis strongly supported the paraphyly of Cobitis and polyphyly of Misgurnus. The strict molecular clock predicted that Cobitinae might have split into northern and southern lineages in the late Eocene (42.11 Ma), furthermore, mtDNA introgression might occur (14.40 Ma) between ancestral species of Cobitis and ancestral species of Misgurnus. Conclusions The current study represents the first comparative mitogenomic and phylogenetic analyses within Cobitinae and provides new insights into the mitogenome features and evolution of fishes belonging to the cobitinae family.

The reversal of human phylogeny: Homo left Africa as erectus, came back as sapiens sapiens

Background The molecular out of Africa hypothesis, OOAH, has been considered as an established fact amid population geneticists for some 25–30 years despite the early concern with it among phylogeneticists with experience beyond that of Homo. The palaeontological support for the hypothesis is also questionable, a circumstance that in the light of expanding Eurasian palaeontological knowledge has become accentuated through the last decades. Results The direction of evolution in the phylogenetic tree of modern humans (Homo sapiens sapiens, Hss) was established inter alia by applying progressive phylogenetic analysis to an mtDNA sampling that included a Eurasian, Lund, and the African Mbuti, San and Yoruba. The examination identified the African populations as paraphyletic, thereby compromising the OOAH. The finding, which was consistent with the out of Eurasia hypothesis, OOEH, was corroborated by the mtDNA introgression from Hss into Hsnn (Neanderthals) that demonstrated the temporal and physical Eurasian coexistence of the two lineages. The results are consistent with the palaeontologically established presence of H. erectus in Eurasia, a Eurasian divergence between H. sapiens and H. antecessor ≈ 850,000 YBP, an Hs divergence between Hss and Hsn (Neanderthals + Denisovans) ≈ 800,000 YBP, an mtDNA introgression from Hss into Hsnn* ≈ 500,000 YBP and an Eurasian divergence among the ancestors of extant Hss ≈ 250,000 YBP at the exodus of Mbuti/San into Africa. Conclusions The present study showed that Eurasia was not the receiver but the donor in Hss evolution. The findings that Homo left Africa as erectus and returned as sapiens sapiens constitute a change in the understanding of Hs evolution to one that conforms to the extensive Eurasian record of Hs palaeontology and archaeology.

Patterns of mtDNA introgression suggest population replacement in Palaearctic whiskered bat species

Secondary contacts can play a major role in the evolutionary histories of species. Various taxa diverge in allopatry and later on come into secondary contact during range expansions. When they meet, their interactions and the extent of gene flow depend on the level of their ecological differentiation and the strength of their reproductive isolation. In this study, we present the multilocus phylogeography of two cryptic whiskered bat species, Myotis mystacinus and M. davidii , with a particular focus on their putative sympatric zone. Our findings suggest that M. mystacinus and M. davidii evolved in allopatry and came into secondary contact during range expansions. Individuals in the area of secondary contact, in Anatolia and the Balkans, have discordant population assignments based on the mitochondrial and the nuclear datasets. These observed patterns suggest that the local M. mystacinus populations hybridized with expanding M. davidii populations, which resulted in mitochondrial introgression from the former. In the introgression area, M. mystacinus individuals with concordant nuclear and mitochondrial genotypes were identified in relatively few locations, suggesting that the indigenous populations might have been largely replaced by invading M. davidii . Changing environmental conditions coupled with ecological competition is the likely reason for this replacement. Our study presents one possible example of a historical population replacement that was captured in phylogeographic patterns.

Introgression obscures lineage boundaries and phylogeographic history in the western banded gecko, Coleonyx variegatus (Squamata: Eublepharidae)

The geomorphological formation of the Baja California peninsula and the Gulf of California is a principal driver of diversification for the reptiles of North America’s warm deserts. The western banded gecko, Coleonyx variegatus, is distributed throughout the Mojave, Sonoran and Peninsular deserts. In this study we use multilocus sequence data to address deep phylogeographic structure within C. variegatus. Analyses of mtDNA data recover six divergent clades throughout the range of C. variegatus. Topology of the mtDNA gene tree suggests separate origins of peninsular populations with an older lineage in the south and a younger one in the north. In contrast, analyses of multilocus nuclear data provide support for four lineages, corresponding to the subspecies C. v. abbotti, C. v. peninsularis, C. v. sonoriensis and C. v. variegatus. Phylogenetic analyses of the nuclear data recover C. v. abbotti and C. v. peninsularis as a clade, indicating a single origin of the peninsular populations. Discordance between the nuclear and mtDNA data is largely the result of repeated episodes of mtDNA introgression that have obscured both lineage boundaries and biogeographic history. Dating analyses of the combined nuclear and mtDNA data suggest that the peninsular clade diverged from the continental group in the Late Miocene.

Ancient hybridization and mtDNA introgression behind current paternal leakage and heteroplasmy in hybrid zones

Hybridization between heterospecific individuals has been documented as playing a direct role in promoting paternal leakage and mitochondrial heteroplasmy in both natural populations and laboratory conditions, by relaxing the egg-sperm recognition mechanisms. Here, we tested the hypothesis that hybridization can lead to mtDNA heteroplasmy also indirectly via mtDNA introgression. By using a phylogenetic approach, we showed in two reproductively isolated beetle species, Ochthebius quadricollis and O. urbanelliae, that past mtDNA introgression occurred between them in sympatric populations. Then, by developing a multiplex allele-specific PCR assay, we showed the presence of heteroplasmic individuals and argue that their origin was through paternal leakage following mating between mtDNA-introgressed and pure conspecific individuals. Our results highlight that mtDNA introgression can contribute to promote paternal leakage, generating genetic novelty in a way that has been overlooked to date. Furthermore, they highlight that the frequency and distribution of mtDNA heteroplasmy can be deeply underestimated in natural populations, as i) the commonly used PCR-Sanger sequencing approach can fail to detect mitochondrial heteroplasmy, and ii) specific studies aimed at searching for it in populations where mtDNA-introgressed and pure individuals co-occur remain scarce, despite the fact that mtDNA introgression has been widely documented in several taxa and populations.