Population-specific signatures of intra-individual mitochondrial DNA heteroplasmy and their potential evolutionary advantages

Heteroplasmy is the existence of more than one mitochondrial DNA (mtDNA) variant within a cell. The evolutionary mechanisms of heteroplasmy are not fully understood, despite being a very common phenomenon. Here we combined heteroplasmy measurements using high throughput sequencing on green turtles (Chelonia mydas) with simulations to understand how heteroplasmy modulates population diversity across generations and under different demographic scenarios. We found heteroplasmy to be widespread in all individuals analysed, with consistent signal in individuals across time and tissue. Significant shifts in haplotype composition were found from mother to offspring, signalling the effect of the cellular bottleneck during oogenesis as included in the model. Our model of mtDNA inheritance indicated that heteroplasmy favoured the increase of population diversity through time and buffered against population bottlenecks, thus indicating the importance of this phenomenon in species with reduced population sizes and frequent population bottlenecks like marine turtles. Individuals with recent haplotypes showed higher levels of heteroplasmy than the individuals with ancient haplotypes, suggesting a potential advantage of maintaining established copies when new mutations arise. We recommend using heteroplasmy through high throughput sequencing in marine turtles, as well as other wildlife populations, for diversity assessment, population genetics, and mixed stock analysis

Geographic patterns of genetic variation in a broadly distributed marine vertebrate: new insights into loggerhead turtle stock structure from expanded mitochondrial DNA sequences

Previous genetic studies have demonstrated that natal homing shapes the stock structure of marine turtle nesting populations. However, widespread sharing of common haplotypes based on short segments of the mitochondrial control region often limits resolution of the demographic connectivity of populations. Recent studies employing longer control region sequences to resolve haplotype sharing have focused on regional assessments of genetic structure and phylogeography. Here we synthesize available control region sequences for loggerhead turtles from the Mediterranean Sea, Atlantic, and western Indian Ocean basins. These data represent six of the nine globally significant regional management units (RMUs) for the species and include novel sequence data from Brazil, Cape Verde, South Africa and Oman. Genetic tests of differentiation among 42 rookeries represented by short sequences (380 bp haplotypes from 3,486 samples) and 40 rookeries represented by long sequences (~800 bp haplotypes from 3,434 samples) supported the distinction of the six RMUs analyzed as well as recognition of at least 18 demographically independent management units (MUs) with respect to female natal homing. A total of 59 haplotypes were resolved. These haplotypes belonged to two highly divergent global lineages, with haplogroup I represented primarily by CC-A1, CC-A4, and CC-A11 variants and haplogroup II represented by CC-A2 and derived variants. Geographic distribution patterns of haplogroup II haplotypes and the nested position of CC-A11.6 from Oman among the Atlantic haplotypes invoke recent colonization of the Indian Ocean from the Atlantic for both global lineages. The haplotypes we confirmed for western Indian Ocean RMUs allow reinterpretation of previous mixed stock analysis and further suggest that contemporary migratory connectivity between the Indian and Atlantic Oceans occurs on a broader scale than previously hypothesized. This study represents a valuable model for conducting comprehensive international cooperative data management and research in marine ecology

Author Correction: Population-specific signatures of intra-individual mitochondrial DNA heteroplasmy and their potential evolutionary advantages

An amendment to this paper has been published and can be accessed via a link at the top of the paper

Data from: Nuclear markers reveal a complex introgression pattern among marine turtle species on the Brazilian coast

A surprisingly high frequency of interspecific sea turtle hybrids have been previously recorded in a nesting site along a short stretch of the Brazilian coast. Mitochondrial DNA data indicated that as much as 43% of the females identified as E. imbricata are hybrids in this area (Bahia State of Brazil). It is a remarkable find, since most of the nesting sites surveyed worldwide, including some in northern Brazil, presents no hybrids, and rare Caribbean sites present no more than 2% of hybrids. Thus, a detailed understanding of the hybridization process is needed to evaluate natural or anthropogenic causes of this regional phenomenon in Brazil, which could be an important factor affecting the conservation of this population. We analyzed a set of 12 nuclear markers to investigate the pattern of hybridization involving three species of sea turtles: hawksbill (Eretmochelys imbricata), loggerhead (Caretta caretta), and olive ridley (Lepidochelys olivacea). Our data indicate that most of the individuals in the crossings L. olivacea × E. imbricata and L. olivacea × C. caretta are F1 hybrids, whereas C. caretta × E. imbricata crossings present F1 and backcrosses with both parental species. In addition, the C. caretta × E. imbricata hybridization seems to be gender and species biased, and we also found one individual with evidence of multispecies hybridization among C. caretta × E. imbricata × Chelonia mydas. The overall results also indicate that hybridization in this area is a recent phenomenon, spanning at least two generations or ~40 years

Individual-by-individual sequence information

The table describes which GenBank accessions numbers came from each individual (smaller database, see article's SI Tab3)

Rag2 fasta alignment

Alignments of Rag2 gene. Sequences are identified as haplotype (see article text for more details) and GenBank number

R35 fasta alignment

Alignment of R35 intron. Sequences are identified as haplotype number (see article text for more details) and GenBank number

Rag1 fasta alignment

Alignments of Rag1 gene. Sequences are identified as haplotype (see article text for more details) and GenBank number

BDNF fasta alignment

Alignments of BDNF gene. Sequences are identified as haplotype number (see article text for more details) and GenBank number

Cmos fasta alignment

Alignment of Cmos gene. Sequences are identified as haplotype number (see article text for more details) and GenBank number