Mitochondrial Introgression Research Articles

Some results of molecular phylogenetic studies of Baikal endemic invertebrates

Baikal and the fauna inhabiting it became an object of systematic evolutionary studies more than a century ago. With the development of the methodical arsenal of biology, almost all approaches were also used to clarify the origin of Baikal’s population. The current review is mainly devoted to the results of using the molecular phylogenetics methods. The exceptional taxonomic wealth of the lake, colossal diversity of biotopes, and wide range of knowledge about different aspects of Baikal’s ecosystem functioning allow us to study such details of speciation mechanisms that are much less accessible in other circumstances. The main common features of modern evolutionary processes in the groups of invertebrates that are rich in species consist in the fact that, at first, most of them are young relative to Baikal and, second, in the fact that the speciation occurs sympatrically, since in spite of its size, the geological history of Baikal lacks episodes of its subdivision long-term enough for allopatric speciation. The reproductive barriers were most likely generated according to the rather complex scenarios developed under the effect of global climatic processes. This resulted in nuclear and mitochondrial introgressions. As a result of this, it is possible that intermediate forms of the organisms are widely distributed in Baikal, and it is very difficult to determine the taxonomic status of many of them. The almost complete absence of experimental evidence of the coevolution of species that are ecologically closely related to each other was also an interesting peculiarity. The results of evolutionary studies mainly devoted to bouquets of species (monophyletic groups of organisms that ensure the exclusively high species diversity of Baikal and the mechanisms of whose development remain largely mysterious) were considered in the review.

Divergent evolutionary histories of DNA markers in a Hawaiian population of the coral Montipora capitata.

We investigated intra- and inter-colony sequence variation in a population of the dominant Hawaiian coral Montipora capitata by analyzing marker gene and genomic data. Ribosomal ITS1 regions showed evidence of a reticulate history among the colonies, suggesting incomplete rDNA repeat homogenization. Analysis of the mitochondrial genome identified a major (M. capitata) and a minor (M. flabellata) haplotype in single polyp-derived sperm bundle DNA with some colonies containing 2–3 different mtDNA haplotypes. In contrast, Pax-C and newly identified single-copy nuclear genes showed either no sequence differences or minor variations in SNP frequencies segregating among the colonies. Our data suggest past mitochondrial introgression in M. capitata, whereas nuclear single-copy loci show limited variation, highlighting the divergent evolutionary histories of these coral DNA markers.

Mitochondrial Recombination and Introgression during Speciation by Hybridization.

Genome recombination is a major source of genotypic diversity and contributes to adaptation and speciation following interspecies hybridization. The contribution of recombination in these processes has been thought to be largely limited to the nuclear genome because organelles are mostly uniparentally inherited in animals and plants, which prevents recombination. Unicellular eukaryotes such as budding yeasts do, however, transmit mitochondria biparentally, suggesting that during hybridization, both parents could provide alleles that contribute to mitochondrial functions such as respiration and metabolism in hybrid populations or hybrid species. We examined the dynamics of mitochondrial genome transmission and evolution during speciation by hybridization in the natural budding yeast Saccharomyces paradoxus. Using population-scale mitochondrial genome sequencing in two endemic North American incipient species SpB and SpC and their hybrid species SpC*, we found that both parental species contributed to the hybrid mitochondrial genome through recombination. We support our findings by showing that mitochondrial recombination between parental types is frequent in experimental crosses that recreate the early step of this speciation event. In these artificial hybrids, we observed that mitochondrial genome recombination enhances phenotypic variation among diploid hybrids, suggesting that it could play a role in the phenotypic differentiation of hybrid species. Like the nuclear genome, the mitochondrial genome can, therefore, also play a role in hybrid speciation.

Perpendicular axes of differentiation generated by mitochondrial introgression.

Differential introgression of mitochondrial vs. nuclear DNA generates discordant patterns of geographic variation and can promote population divergence and speciation. We examined a potential case of mitochondrial introgression leading to two perpendicular axes of differentiation. The Eastern Yellow Robin Eopsaltria australis, a widespread Australian bird, shows a deep mitochondrial split that is perpendicular to north-south nuclear DNA and plumage colour differentiation. We propose a scenario to explain this pattern: (i) first, both nuclear and mitochondrial genomes differentiated in concert during north-south population divergence; (ii) later, their histories disconnected after two mitochondrial introgression events resulting in a deep mitochondrial split perpendicular to the nuclear DNA structure. We explored this scenario by coalescent modelling of ten mitochondrial genes and 400 nuclear DNA loci. Initial mitochondrial and nuclear genome divergences were estimated to have occurred in the early Pleistocene, consistent with the proposed scenario. Subsequent climatic transitions may have driven later mitochondrial introgression. We consider neutral introgression unlikely and instead propose that the evidence is more consistent with adaptive mitochondrial introgression and selection against incompatible mitochondrial-nuclear combinations. This likely generated an axis of coastal-inland mitochondrial differentiation in the face of nuclear gene flow, perpendicular to the initial north-south axis of differentiation (reflected in genomewide nuclear DNA and colour variation).

Taming the late Quaternary phylogeography of the Eurasiatic wild ass through ancient and modern DNA.

Taxonomic over-splitting of extinct or endangered taxa, due to an incomplete knowledge of both skeletal morphological variability and the geographical ranges of past populations, continues to confuse the link between isolated extant populations and their ancestors. This is particularly problematic with the genus Equus. To more reliably determine the evolution and phylogeographic history of the endangered Asiatic wild ass, we studied the genetic diversity and inter-relationships of both extinct and extant populations over the last 100,000 years, including samples throughout its previous range from Western Europe to Southwest and East Asia. Using 229 bp of the mitochondrial hypervariable region, an approach which allowed the inclusion of information from extremely poorly preserved ancient samples, we classify all non-African wild asses into eleven clades that show a clear phylogeographic structure revealing their phylogenetic history. This study places the extinct European wild ass, E. hydruntinus, the phylogeny of which has been debated since the end of the 19th century, into its phylogenetic context within the Asiatic wild asses and reveals recent mitochondrial introgression between populations currently regarded as separate species. The phylogeographic organization of clades resulting from these efforts can be used not only to improve future taxonomic determination of a poorly characterized group of equids, but also to identify historic ranges, interbreeding events between various populations, and the impact of ancient climatic changes. In addition, appropriately placing extant relict populations into a broader phylogeographic and genetic context can better inform ongoing conservation strategies for this highly-endangered species.

Microsatellite analysis supports the existence of three cryptic species within the bumble bee Bombus lucorum sensu lato

Mitochondrial cytochrome oxidase I (COI) partial sequences are widely used in taxonomy for species identification. Increasingly, these sequence identities are combined with modelling approaches to delineate species. Yet the validity of species delineation based on such DNA ‘barcodes’ is rarely tested and may be called into question by phenomena such as ancestral polymorphisms in DNA sequences, phylogeographic divergence, mitochondrial introgression and hybridization, or distortion of mitochondrial inheritance through such factors as Wolbachia infection. The common and widespread European bumble bee Bombus lucorum s. lato contains three distinct mitochondrial DNA lineages that are assumed to represent three cryptic species, namely Bombus cryptarum, B. lucorum s. str. and B. magnus. To test whether nuclear gene pools of the three putative species were differentiated, we genotyped 304 sympatric members of the lucorum complex (54 B. cryptarum females, 168 B. lucorum s. str. females and 82 B. magnus females, as defined using mtDNA COI haplotypes) from 11 localities spread across the island of Ireland at seven nuclear microsatellite loci. Multilocus genotypes clustered into three discrete groups that largely corresponded to the three mtDNA lineages: B. cryptarum, B. lucorum s. str. and B. magnus. The good fit of mitochondrial haplotype to nuclear (microsatellite) genotypic data supports the view that these three bumble bee taxa are reproductively isolated species, as well as providing a vindication of species identity using so-called DNA barcodes.

When different contact zones tell different stories: putative ring species in the Megachile concinna species complex (Hymenoptera: Megachilidae)

We examine the genetics, morphology and ecology of the widely distributed Megachile concinna species complex (Hymenoptera: Megachilidae), which is composed of numerous taxa of unclear taxonomic status in Africa and the Palearctic. In the Western Palearctic, three genetically distinct operational taxonomic units (OTUs) are found around the Mediterranean Sea: the western Mediterranean OTU M. pusilla, the eastern Mediterranean OTU M. anatolica and the predominantly Arabian OTU M. leucostoma. A morphological cline is present between anatolica and leucostoma in the Near East, despite a lack of mitochondrial introgression between the two; one nuclear marker suggests some gene flow between these OTUs. The contact zone between pusilla and leucostoma could not be sampled but phenotypic intergradation is also observed between these OTUs in northern Africa. In contrast, study of the contact zone between pusilla and anatolica indicates that both OTUs retain phenotypic and genomic integrity in sympatry over a contact zone spanning 1000 km. The arrangement of these three OTUs suggests a ring of interconnected populations around the Mediterranean Sea and sympatry between pusilla and anatolica at both ends of the ring in southeastern Europe. The latter two OTUs exhibit ecological differences, including phenology and host-plant preferences, which may contribute to their isolation. In addition, our results suggest that two OTUs, M. venusta and M. concinna, maintain genetic and phenotypic integrity in sympatry in parts of Africa; the latter is recognized as a valid species here. Lastly, our results indicate that two OTUs have been introduced independently into the New World, pusilla in North America and Argentina, and concinna in the Antilles.

Historical introgression drives pervasive mitochondrial admixture between two species of pelagic sharks

We use a genomic sampling of both nuclear and mitochondrial DNA markers to examine a pattern of genetic admixture between Carcharhinus galapagensis (Galapagos sharks) and Carcharhinus obscurus (dusky sharks), two well-known and closely related sharks that have been recognized as valid species for more than 100years. We describe widespread mitochondrial-nuclear discordance in which these species are readily distinguishable based on 2152 nuclear single nucleotide polymorphisms from 910 independent autosomal regions, but show pervasive mitochondrial admixture. The species are superficially morphologically cryptic as adults but show marked differences in internal anatomy, as well as niche separation. There was no indication of ongoing hybridization between the species. We conclude that the observed mitochondrial-nuclear discordance is likely due to historical mitochondrial introgression following a range expansion.

Mitochondrial introgression suggests extensive ancestral hybridization events among Saccharomyces species

Horizontal gene transfer (HGT) in eukaryotic plastids and mitochondrial genomes is common, and plays an important role in organism evolution. In yeasts, recent mitochondrial HGT has been suggested between S. cerevisiae and S. paradoxus. However, few strains have been explored given the lack of accurate mitochondrial genome annotations. Mitochondrial genome sequences are important to understand how frequent these introgressions occur, and their role in cytonuclear incompatibilities and fitness. Indeed, most of the Bateson-Dobzhansky-Muller genetic incompatibilities described in yeasts are driven by cytonuclear incompatibilities. We herein explored the mitochondrial inheritance of several worldwide distributed wild Saccharomyces species and their hybrids isolated from different sources and geographic origins. We demonstrated the existence of several recombination points in mitochondrial region COX2-ORF1, likely mediated by either the activity of the protein encoded by the ORF1 (F-SceIII) gene, a free-standing homing endonuclease, or mostly facilitated by A+T tandem repeats and regions of integration of GC clusters. These introgressions were shown to occur among strains of the same species and among strains of different species, which suggests a complex model of Saccharomyces evolution that involves several ancestral hybridization events in wild environments.

When COI barcodes deceive: complete genomes reveal introgression in hairstreaks.

Two species of hairstreak butterflies from the genus Calycopis are known in the United States: C. cecrops and C. isobeon Analysis of mitochondrial COI barcodes of Calycopis revealed cecrops-like specimens from the eastern US with atypical barcodes that were 2.6% different from either USA species, but similar to Central American Calycopis species. To address the possibility that the specimens with atypical barcodes represent an undescribed cryptic species, we sequenced complete genomes of 27 Calycopis specimens of four species: C. cecrops, C. isobeon, C. quintana and C. bactra Some of these specimens were collected up to 60 years ago and preserved dry in museum collections, but nonetheless produced genomes as complete as fresh samples. Phylogenetic trees reconstructed using the whole mitochondrial and nuclear genomes were incongruent. While USA Calycopis with atypical barcodes grouped with Central American species C. quintana by mitochondria, nuclear genome trees placed them within typical USA C. cecrops in agreement with morphology, suggesting mitochondrial introgression. Nuclear genomes also show introgression, especially between C. cecrops and C. isobeon About 2.3% of each C. cecrops genome has probably (p-value < 0.01, FDR < 0.1) introgressed from C. isobeon and about 3.4% of each C. isobeon genome may have come from C. cecrops. The introgressed regions are enriched in genes encoding transmembrane proteins, mitochondria-targeting proteins and components of the larval cuticle. This study provides the first example of mitochondrial introgression in Lepidoptera supported by complete genome sequencing. Our results caution about relying solely on COI barcodes and mitochondrial DNA for species identification or discovery.

Phylogenetic analysis of the genus Laparocerus, with comments on colonisation and diversification in Macaronesia (Coleoptera, Curculionidae, Entiminae).

The flightless Entiminae weevil genus Laparocerus is the species-richest genus, with 237 species and subspecies, inhabiting Macaronesia (Madeira archipelago, Selvagens, Canary Islands) and the continental ‘Macaronesian enclave’ in Morocco (one single polytypic species). This is the second contribution to gain insight of the genus and assist in its systematic revision with a mitochondrial phylogenetic analysis. It centres on the Canarian clade, adding the 12S rRNA gene to the combined set of COII and 16S rRNA used in our first contribution on the Madeiran clade (here re-analysed). The nuclear 28S rRNA was also used to produce an additional 4-gene tree to check coherency with the 3-gene tree.A total of 225 taxa (95%) has been sequenced, mostly one individual per taxa. Plausible explanations for incoherent data (mitochondrial introgressions, admixture, incomplete lineage sorting, etc.) are discussed for each of the monophyletic subclades that are coincident with established subgenera, or are restructured or newly described. The overall mean genetic divergence (p-distance) among species is 8.2%; the mean divergence within groups (subgenera) ranks from 2.9 to 7.0% (average 4.6%), and between groups, from 5.4% to 12.0% (average 9.2%). A trustful radiation event within a young island (1.72 Ma) was used to calibrate and produce a chronogram using the software RelTime.These results confirm the monophyly of both the Madeiran (36 species and subspecies) and the Canarian (196 species and subspecies) clades, which originated ca. 11.2 Ma ago, and started to radiate in their respective archipelagos ca. 8.5 and 7.7 Ma ago. The Madeiran clade seems to have begun in Porto Santo, and from there it jumped to the Desertas and to Madeira, with additional radiations. The Canarian clade shows a sequential star-shape radiation process generating subclades with a clear shift from East to West in coherence with the decreasing age of the islands. Laparocerus garretai from the Selvagens belongs to a Canarian subclade, and Laparocerus susicus from Morocco does not represent the ancestral continental lineage, but a back-colonisation from the Canaries to Africa. Dispersal processes, colonisation patterns, and ecological remarks are amply discussed. Diversification has been adaptive as well as non-adaptive, and the role of ’geological turbulence’ is highlighted as one of the principal drivers of intra-island allopatric speciation.Based on the phylogenetic results, morphological features and distribution, five new monophyletic subgenera are described: Aridotrox subg. n., Belicarius subg. n., Bencomius subg. n., Canariotrox subg. n., and Purpuranius subg. n., totalling twenty subgenera in Laparocerus.

The on-again, off-again relationship between mitochondrial genomes and species boundaries.

The study of reproductive isolation and species barriers frequently focuses on mitochondrial genomes and has produced two alternative and almost diametrically opposed narratives. On one hand, mtDNA may be at the forefront of speciation events, with co-evolved mitonuclear interactions responsible for some of the earliest genetic incompatibilities arising among isolated populations. On the other hand, there are numerous cases of introgression of mtDNA across species boundaries even when nuclear gene flow is restricted. We argue that these seemingly contradictory patterns can result from a single underlying cause. Specifically, the accumulation of deleterious mutations in mtDNA creates a problem with two alternative evolutionary solutions. In some cases, compensatory or epistatic changes in the nuclear genome may ameliorate the effects of mitochondrial mutations, thereby establishing coadapted mitonuclear genotypes within populations and forming the basis of reproductive incompatibilities between populations. Alternatively, populations with high mitochondrial mutation loads may be rescued by replacement with a more fit, foreign mitochondrial haplotype. Coupled with many nonadaptive mechanisms of introgression that can preferentially affect cytoplasmic genomes, this form of adaptive introgression may contribute to the widespread discordance between mitochondrial and nuclear genealogies. Here, we review recent advances related to mitochondrial introgression and mitonuclear incompatibilities, including the potential for cointrogression of mtDNA and interacting nuclear genes. We also address an emerging controversy over the classic assumption that selection on mitochondrial genomes is inefficient and discuss the mechanisms that lead lineages down alternative evolutionary paths in response to mitochondrial mutation accumulation.

Ancient and modern genome shuffling: Reticulate mito-nuclear phylogeny of four related allopatric species of Gyrodactylus von Nordmann, 1832 (Monogenea: Gyrodactylidae), ectoparasites on the Eurasian minnow Phoxinus phoxinus (L.) (Cyprinidae).

Phylogenetic analyses including four allopatric species of Gyrodactylus von Nordmann, 1832 on the Eurasian minnow Phoxinus phoxinus (L.) (Cyprinidae) revealed incongruence between the nuclear ITS1-5.8S-ITS2 and mitochondrial cox1 phylogenies due to ancient hybridisation. Gyrodactylus pannonicus Molnár, 1968 was sampled close to its type-locality, the upper reaches of River Tisza, tributary of Danube in the Black Sea Basin. Faunistic search detected three new related species with maximum composite likelihood distances in cox1 between 16.8-23.2% (tentatively 1.3 to 1.8 My of divergence). Gyrodactylus albolacustris n. sp. recorded in the White Sea Basin, eastern Baltic Basin and Mongolia was close to G. pannonicus in the nuclear ITS (divergence of 0.9%), but diverged in cox1 by 19.8%. The Mongolian isolate of G. albolacustris n. sp. diverged from the European isolates in cox1 by 8.9%, suggesting 0.7My of isolation. The two other new species differed from G. pannonicus by>4% in ITS and some large indels in ITS1, and by>20% in cox1. Gyrodactylus danastriae n. sp. was found in River Strwiąż, a tributary of the River Dniester (Black Sea Basin) and was characterised by smaller size of anchors and by 29-41bp dimorphic insertion in ITS1. Gyrodactylus botnicus n. sp. is considered endemic in the Baltic Basin, but was also found in the White Sea Basin as a postglacial immigrant, where it had hybridised with G. albolacustris n. sp. in spite of the high divergence in ITS (3.9%) and cox1 (22%). The discordant nuclear and mitochondrial phylogenies revealed an ancient mitochondrial introgression: G. albolacustris n. sp. was derived from a hybridisation combining proto-pannonicus ITS with proto-danastriae mitochondria, perhaps 1.3 My ago. The postglacial hybridisation of G. albolacustris n. sp. (as the donor of mtDNAalb and ITSalb) and G. botnicus n. sp. (donor of the ITSbot) offered a model of shuffling of the genomic components: the process of the homogenisation and stabilisation of nuclear ITS (concerted evolution) and the lineage sorting has hardly begun.

The birth of aposematism: High phenotypic divergence and low genetic diversity in a young clade of poison frogs

Rapid radiation coupled with low genetic divergence often hinders species delimitation and phylogeny estimation even if putative species are phenotypically distinct. Some aposematic species, such as poison frogs (Dendrobatidae), have high levels of intraspecific color polymorphism, which can lead to overestimation of species when phenotypic divergence primarily guides species delimitation. We explored this possibility in the youngest origin of aposematism (3–7 MYA) in poison frogs, Epipedobates, by comparing genetic divergence with color and acoustic divergence. We found low genetic divergence (2.6% in the 16S gene) despite substantial differences in color and acoustic signals. While chemical defense is inferred to have evolved in the ancestor of Epipedobates, aposematic coloration evolved at least twice or was lost once in Epipedobates, suggesting that it is evolutionarily labile. We inferred at least one event of introgression between two cryptically colored species with adjacent ranges (E. boulengeri and E. machalilla). We also find evidence for peripheral isolation resulting in phenotypic divergence and potential speciation of the aposematic E. tricolor from the non-aposematic E. machalilla. However, we were unable to estimate a well-supported species tree or delimit species using multispecies coalescent models. We attribute this failure to factors associated with recent speciation including mitochondrial introgression, incomplete lineage sorting, and too few informative molecular characters. We suggest that species delimitation within young aposematic lineages such as Epipedobates will require genome-level molecular studies. We caution against relying solely on DNA barcoding for species delimitation or identification and highlight the value of phenotypic divergence and natural history in delimiting species.

Improved sampling at the subspecies level solves a taxonomic dilemma – A case study of two enigmatic Chinese tit species (Aves, Passeriformes, Paridae, Poecile)

A recent full species-level phylogeny of tits, titmice and chickadees (Paridae) has placed the Chinese endemic black-bibbed tit (Poecile hypermelaenus) as the sister to the Palearctic willow tit (P. montanus). Because this sister-group relationship is in striking disagreement with the traditional affiliation of P. hypermelaenus close to the marsh tit (P. palustris) we tested this phylogenetic hypothesis in a multi-locus analysis with an extended taxon sampling including sixteen subspecies of willow tits and marsh tits. As a taxonomic reference we included type specimens in our analysis. The molecular genetic study was complemented with an analysis of biometric data obtained from museum specimens. Our phylogenetic reconstructions, including a comparison of all GenBank data available for our target species, clearly show that the genetic lineage previously identified as P. hypermelaenus actually refers to P. weigoldicus because sequences were identical to that of a syntype of this taxon. The close relationship of P. weigoldicus and P. montanus – despite large genetic distances between the two taxa – is in accordance with current taxonomy and systematics. In disagreement with the previous phylogenetic hypothesis but in accordance with most taxonomic authorities, all our P. hypermelaenus specimens fell in the sister clade of all western and eastern Palearctic P. palustris. Though shared haplotypes among the Chinese populations of the two latter species might indicate mitochondrial introgression in this part of the breeding range, further research is needed here due to the limitations of our own sampling.

Ancient Mitochondrial Capture as Factor Promoting Mitonuclear Discordance in Freshwater Fishes: A Case Study in the Genus Squalius (Actinopterygii, Cyprinidae) in Greece.

Hybridization and incomplete lineage sorting are common confounding factors in phylogeny and speciation resulting in mitonuclear disparity. Mitochondrial introgression, a particular case of hybridization, may, in extreme cases, lead to replacement of the mitochondrial genome of one species with that of another (mitochondrial capture). We investigated mitochondrial introgression involving two species of the cyprinid genus Squalius in the western Peloponnese region of Greece using molecular and morphological data. We found evidence of complete mitochondrial introgression of Squalius keadicus into two populations recognized as Squalius peloponensis from the Miras and Pamissos River basins and a divergence of mitochondrial genomes of S. keadicus from the Evrotas basin from that of the introgressed populations dating from the Pleistocene. Secondary contact among basins is a possible factor in connection of the species and the introgression event. Morphological analyses support the hypothesis of mitochondrial introgression, as S. keadicus was different from the other three populations recognized as S. peloponensis, although significant differences were found among the four populations. Isolation by geographical barriers arose during Pleistocene in the western Peloponnese were the source of the evolution of the two reciprocally monophyletic subclades found in the S. keadicus mitochondrial clade, and the morphological differences found among the four populations. Along with the lack of structure in the nuclear genome in the three populations ascribed to S. peloponensis, this suggests an incipient speciation process occurring in these Squalius species in the western Peloponnese.

Multilocus approaches reveal underestimated species diversity and inter-specific gene flow in pikas (Ochotona) from southwestern China

The phylogeny of living pikas (Ochotonidae, Ochotona) remains obscure, and pika species diversity in southwestern China has never been well explored. In this study, 96 tissue samples from 11 valid species in three classified subgenera (Pika, Ochotona and Conothoa) from 23 locations were characterized using multilocus sequences of 7031bp. Two mitochondrial (CYT B and COI) and five nuclear gene segments (RAG1, RAG2, TTN, OXAIL and IL1RAPL1) were sequenced. We analysed evolutionary histories using maximum likelihood (RAxML) and Bayesian analyses (BEAST), and we also used molecular species delimitation analyses (BPP) to explore species diversity. Our study supported O. syrinx (O. huangensis) as a distinct clade from all named subgenera. Relationships among subgenera were not fully resolved, which may be due to a rapid diversification in the middle Miocene (∼13.90Ma). Conflicting gene trees implied mitochondrial introgression from O. cansus to O. curzoniae. We uncovered three cryptic species from Shaanxi, Sichuan and Yunnan with strong support, suggesting an underestimation of species diversity in the “sky-island” mountains of southwest China.

Combined hybridization and mitochondrial capture shape complex phylogeographic patterns in hybridogenetic Cataglyphis desert ants

Some species of Cataglyphis desert ants have evolved a hybridogenetic mode of reproduction at the social scale. In hybridogenetic populations, two distinct genetic lineages coexist. Non-reproductive offspring (workers) are hybrids of the two lineages, whereas sexual offspring (males and new queens) are produced by parthenogenesis and belong to the mother queen lineage. How this unusual reproductive system affects phylogeographic patterns and speciation processes remains completely unknown to date. Using one mitochondrial and four nuclear genes, we examined the phylogenetic relationships between three species of Cataglyphis (C. hispanica, C. humeya and C. velox) where complex DNA inheritance through social hybridogenesis may challenge phylogenetic inference. Our results bring two important insights. First, our data confirm a hybridogenetic mode of reproduction across the whole distribution range of the species C. hispanica. In contrast, they do not provide support for hybridogenesis in the populations sampled of C. humeya and C. velox. This suggests that these populations are not hybridogenetic, or that hybridogenesis is too recent to result in reciprocally monophyletic lineages on nuclear genes. Second, due to mitochondrial introgression between lineages (Darras and Aron, 2015), the faster-evolving COI marker is not lineage specific, hence, unsuitable to further investigate the segregation of lineages in the species studied. Different mitochondrial haplotypes occur in each locality sampled, resulting in strongly structured populations. This micro-allopatric structure leads to over-splitting species delimitation on mitochondrial gene, as every locality could potentially be considered a putative species; haploweb analyses of nuclear markers, however, yield species delimitations that are consistent with morphology. Overall, this study highlights how social hybridogenesis varies across species and shapes complex phylogeographic patterns.

Do genes lie? Mitochondrial capture masks the Red Sea collector urchin’s true identity (Echinodermata: Echinoidea: Tripneustes)

Novel COI and bindin sequences of the Red Sea collector echinoid Tripneustes gratilla elatensis are used to show that (1) discordance between mitochondrial and nuclear loci exists in this echinoid genus, (2) Tripneustes gratilla as currently defined possibly comprises a complex of cryptic species, and (3) Red Sea Tripneustes form a genetically distinct clade in the bindin tree, which diverged from other Tripneustes clades at least 2–4million years ago. Morphological reassessment of T. gratilla elatensis shows perfect congruence between identification based on skeletal features and genetic data based on a nuclear marker sequence. Hence the Red Sea Tripneustes subspecies established by Dafni in 1983 is a distinct biological unit.All T. g. elatensis samples analyzed are highly similar to or share mtDNA haplotypes with Philippine T. g. gratilla, as do representatives from other edge-of-range occurrences. This lack of genetic structure in Indo-Pacific Tripneustes is interpreted as a result of wide-spread mitochondrial introgression. New fossil specimens from the Red Sea area confirm the sympatric occurrence of T. g. elatensis and T. g. gratilla in the northern Red Sea during Late Pleistocene, identifying a possible timing for the introgression. In addition, present-day distribution shows a contact zone in the Southern Red Sea (in the Dahlak Archipelago).T. g. elatensis, is yet another example of a Red Sea taxon historically identified as conspecific with its Indo-Pacific relatives, but which turned out to be a morphologically and genetically distinct endemic taxon, suggesting that the level of endemism in the Red Sea may still be underestimated.

Dynamics of mtDNA introgression during species range expansion: insights from an experimental longitudinal study.

Introgressive hybridization represents one of the long-lasting debated genetic consequences of species range expansion. Mitochondrial DNA has been shown to heavily introgress between interbreeding animal species that meet in new sympatric areas and, often, asymmetric introgression from local to the colonizing populations has been observed. Disentangling among the evolutionary and ecological processes that might shape this pattern remains difficult, because they continuously act across time and space. In this context, long-term studies can be of paramount importance. Here, we investigated the dynamics of mitochondrial introgression between two mosquito species (Aedes mariae and Ae. zammitii ) during a colonization event that started in 1986 after a translocation experiment. By analyzing 1,659 individuals across 25 years, we showed that introgression occurred earlier and at a higher frequency in the introduced than in the local species, showing a pattern of asymmetric introgression. Throughout time, introgression increased slowly in the local species, becoming reciprocal at most sites. The rare opportunity to investigate the pattern of introgression across time during a range expansion along with the characteristics of our study-system allowed us to support a role of demographic dynamics in determining the observed introgression pattern.