The formation of continental Europe in the Neogene was due to the regression of the Tethys Ocean and of the Paratethys Sea. The dynamic geology of the area and repetitious transitions between marine and freshwater conditions presented opportunities for the colonization of newly emerging hydrological networks and diversification of aquatic biota. Implementing mitochondrial and nuclear markers in conjunction with a large-scale sampling strategy, we investigated the impact of this spatiotemporal framework on the evolutionary history of a freshwater crustacean morphospecies. The Gammarus balcanicus species complex is widely distributed in the area previously occupied by the Paratethys Sea. Our results revealed its high diversification and polyphyly in relation to a number of other morphospecies. The distribution of the studied amphipod is generally characterized by very high local endemism and divergence. The Bayesian time-calibrated reconstruction of phylogeny and geographical distribution of ancestral nodes indicates that this species complex started to diversify in the Early Miocene in the central Balkans, partially in the shallow epicontinental sea. It is possible that there were several episodes of inland water colonization by local brackish water lineages. Subsequent diversification within clades and spread to new areas could have been induced by Alpine orogeny in the Miocene/Pliocene and, finally, by Pleistocene glaciations. The present distribution of clades, in many cases, still reflects Miocene palaeogeography of the area. Our results point out that investigations of the historical aspect of cryptic diversity in other taxa may help in a general understanding of the origins of freshwater invertebrate fauna of Europe.
A number of studies have claimed that recombination occurs in animal mtDNA, although this evidence is controversial. Ladoukakis and Zouros (2001) provided strong evidence for mtDNA recombination in the COIII gene in gonadal tissue in the marine mussel Mytilus galloprovincialis from the Black Sea. The recombinant molecules they reported had not however become established in the population from which experimental animals were sampled. In the present study, we provide further evidence of the generality of mtDNA recombination in Mytilus by reporting recombinant mtDNA molecules in a related mussel species, Mytilus trossulus, from the Baltic. The mtDNA region studied begins in the 16S rRNA gene and terminates in the cytochrome b gene and includes a major noncoding region that may be analogous to the D-loop region observed in other animals. Many bivalve species, including some Mytilus species, are unusual in that they have two mtDNA genomes, one of which is inherited maternally (F genome) the other inherited paternally (M genome). Two recombinant variants reported in the present study have population frequencies of 5% and 36% and appear to be mosaic for F-like and M-like sequences. However, both variants have the noncoding region from the M genome, and both are transmitted to sperm like the M genome. We speculate that acquisition of the noncoding region by the recombinant molecules has conferred a paternal role on mtDNA genomes that otherwise resemble the F genome in sequence.
Many bivalve species, including mussels of the genus Mytilus, are unusual in having two mtDNA genomes, one inherited maternally (the F genome) and the other inherited paternally (the M genome). The sequence differences between the genomes are usually great, indicating ancient divergence predating speciation events. However, in Mytilus trossulus from the Baltic, both genomes are similar to the F genome from the closely related M. edulis. This study analyzed the mtDNA control region structure in male and female Baltic M. trossulus mussels. We show that a great diversity of structural rearrangements is present in both sexes. Sperm samples are dominated by recombinant haplotypes with M. edulis M-like control region segments, some having large duplications. By contrast, the rearranged haplotypes that dominate in eggs lack segments from this M genome. The rearrangements can be explained by a combination of tandem duplication, deletion, and intermolecular recombination. An evolutionary pathway leading to the recombinant haplotypes is suggested. The data are also considered in relation to the hypothesis that the M. edulis M-like control region sequence is necessary to confer the paternal role on genomes that are otherwise F-like. S TRICTLY uniparental inheritance of organelle genomes is a rule in nearly all anisogamic organisms. One of the most prominent exceptions is the mitochondrial inheritance system of mussels of the family Mytilidae in which separate maternal (the F genome) and paternal (the M genome) routes of mtDNA inheritance occur (for review, see Skibinski et al.1994a,b; Zouros et al. 1994a,b;Zouros 2000). This system, called doubly uniparental inheritance (DUI) (Zouros et al. 1994a), has also been observed in freshwater mussels of the family Unionidae (Hoeh et al. 1996;Liu et al. 1996) and clams of the family Veneridae (Passamonti and Scali 2001). Phylogenetic analysis indicates that divergence of the F and M genomes can be great, predating speciation events, and that role reversal or masculinization events, whereby the F genome takes on the role of the previous M genome, has occurred repeatedly in the evolution of marine mussels (Hoeh et al. 1996(Hoeh et al. , 1997, but is absent or less frequent in freshwater mussels (Hoeh et al. 2002).A hybrid zone separates Baltic Mytilus trossulus from North Sea M. edulis populations (see Riginos and Cunningham 2005 for review). Although there is little introgression of mtDNA between American M. trossulus and M. edulis (Saavedra et al. 1996;Comesana et al. 1999) in Baltic M. trossulus, the mtDNA in heteroplasmic male individuals is similar to that in the F genome from M. edulis (Quesada et al. 1995(Quesada et al. , 2003Wenne and Skibinski 1995; Zbawicka et al. 2003a,b). It appears that there has been complete asymmetric introgression of M. edulis F mtDNA into Baltic M. trossulus, accompanied by role reversal and masculinization (Rawson and Hilbish 1998;Quesada et al. 1999). These processes might be coupled and associated with cytonuclear incompatibilities that ...
Summary Pleistocene glaciations affected the present‐day distribution and genetic diversity of animal species in Europe. Deep genetic subdivisions observed in European populations of the widespread freshwater isopod morphospecies, Asellus aquaticus, suggest the presence of putative cryptic species. We used the DNA barcodes of the cytochrome c oxidase subunit 1 (COI) gene combined with distance‐ and tree‐based methods of species delimitation as a rapid tool for assessing the number of distinct operational taxonomic units (OTUs) representing potential cryptic species. The spatial and demographic aspect of A. aquaticus distribution was also analysed. We generated a tentative temporal framework for diversification within the morphospecies provided by the molecular clock approach. Altogether, our study included 603 COI sequences from 147 populations from all over Europe and Asia Minor, including the already published data deposited in GenBank. The mtDNA‐based phylogenetic and OTU delimitation pattern was assessed with results of the nuclear data set analysis including the sequence data derived from this study and those previously submitted in GenBank. In total, 16 haplotypes of 28S rDNA were used representing all COI‐based OTUs and 53 localities. Our results show that A. aquaticus is a conglomerate of genetically distinct COI OTUs. One of the OTUs seems to correspond to the nominative subspecies of A. aquaticus aquaticus, recently redescribed from Sweden, and another with the recently described A. kosswigi. Most of the OTUs are probably of pre‐Pleistocene origin and have narrow ranges in southern Europe. A recent expansion, in both demographic and spatial terms, was revealed in one OTU, which is widely distributed in Europe and represents A. aquaticus aquaticus. This may be explained by the post‐glacial recolonisation processes. According to our data, this OTU probably emerged and initially diversified in the west Balkans in the Middle/Late Pliocene with several lineages surviving and diversifying through the Pleistocene glaciations and expanding during the interglacials. In some cases, our 28S data support the COI‐based OTUs and provide ample evidence for the existence of distinct OTUs, especially in mountainous and karst areas. However, other COI OTUs are not reciprocally monophyletic with respect to nuclear marker. This phylogenetic pattern can be interpreted predominantly as a result of incomplete sorting of nuclear lineages, potentially indicating an ongoing speciation process, but also as an effect of introgression resulting from secondary contact of formerly peripatric or allopatric mitochondrial lineages.
The unusual mode of mitochondrial DNA inheritance, with two separate: maternal (F) and paternal (M) lineages, gives unique opportunities to study the evolution of the mitochondrial genome. This system was first discovered in the marine mussels Mytilus. The three related species: Mytilus edulis, Mytilus galloprovincialis and Mytilus trossulus form a complex in which the divergence of M and F lineages pre-dates the speciation. The complete mitochondrial genomes of both lineages were known for all species except Pacific M. trossulus. Here we report, for the first time, the complete sequences of both mitochondrial genomes of Pacific M. trossulus, filling the gap. While the reported M and F genomes are highly diverged (26%), they have similar organisation. The only difference is the translocation of one tRNA gene into the long, mosaic control region of the F genome. Consistent presence of an ORF which most likely represents the atp8 gene was confirmed in both genomes. The predicted protein has characteristics expected of the functional atp8 even though the M and F versions are markedly different in length. Comparative analysis involving all three species led to the conclusion that the cause of a faster evolution of atp8 and Mytilus mtDNA in general is most likely the Compensation-Draft Feedback process coupled with relatively relaxed selection in the M lineage. Thus, we postulate that the adaptive changes may have played a role in the emergence of highly diverged, barely recognizable atp8 in Mytilus mussels.
Aim Lake Ohrid is the oldest existing lake in Europe, dating back to the Tertiary. Given its surface area and the adjusted endemism rate, it seems to hold the greatest biodiversity of any ancient lake. Of all the animal groups endemic to this lake, gammarids form one of the largest species flocks. The goal of our study was (1) to develop the phylogenetic framework for the Ohridian endemic Gammarus species flock and place it within a regional palaeobiogeographical context, and (2) to interpret the data with respect to the putative origin of the Lake Ohrid fauna. Location Lake Ohrid, Balkan Peninsula. Methods Sequences of two mitochondrial genes (cytochrome c oxidase subunit I and 16S ribosomal RNA) and one nuclear gene (28S ribosomal RNA) of the Ohridian endemic Gammarus species and of other Balkan gammarids from 69 localities were analysed. The phylogenetic relationships of the group were studied using Bayesian methods. The biogeographical history and the chronology of diversification events were investigated using a relaxed molecular clock with two calibration points. Results It appears that the Lake Ohrid gammarids derive from an old local lineage of the Gammarus balcanicus complex. This lineage arrived from the northern part of the Proto‐Balkans, after its emergence during the Tethys/Paratethys regression, and differentiated during the last 18 Myr of the Dinaric uplift (Alpine orogeny). It is also closely affiliated with the biota endemic to the neighbouring area of the former Miocene lake system and to lineages from the upper Vardar and Črni Drim river systems. Main conclusions The Lake Ohrid endemic fauna is closely affiliated to the local biota and its roots are more ancient than the lake itself.
Recombination in the control region (CR) of Mytilus mitochondrial DNA (mtDNA) was originally reported based on the relatively short, sequenced fragments of mitochondrial genomes. Recombination outside the CR has been reported recently with the suggestion that such processes are common in Mytilus. We have fully sequenced a set of 11 different mitochondrial haplotypes representing the high diversity of paternally inherited mitochondrial genomes of Baltic Sea Mytilus mussels, including the haplotype close to the native Mytilus trossulus mitochondrial genome, which was thought to have been entirely eliminated from this population. Phylogenetic and comparative analysis showed that the recombination is limited to the vicinity of the CR in all sequenced genomes. Coding sequence comparison indicated that all paternally inherited genomes showed increased accumulation of nonsynonymous substitutions, including the genomes which switched their transmission route very recently. The acquisition of certain CR sequences through recombination with highly divergent paternally inherited genomes seems to precede and favor the switch, but it is not a prerequisite for this process. Interspecies hybridization in the Baltic Sea during the recent 10,000 years created conditions for both structural and evolutionary mitochondrial instability which resulted in the observed variation and dynamics of mtDNA in Baltic Sea Mytilus mussels. In conclusion, the data shows that the effects of mitochondrial recombination are limited to the CR of few phylogenetic lineages.Electronic supplementary materialThe online version of this article (doi:10.1007/s00438-014-0888-3) contains supplementary material, which is available to authorized users.
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