Highly polymorphic mitochondrial DNA and deceiving haplotypic differentiation: implications for assessing population genetic differentiation and connectivity

Abstract

Background Hyperdiverse mtDNA with more than 5% of variable synonymous nucleotide sites can lead to erroneous interpretations of population genetic differentiation patterns and parameters (φ ST , D EST ). We illustrate this by using hyperdiverse mtDNA markers to infer population genetic differentiation and connectivity in Melarhaphe neritoides , a NE Atlantic (NEA) gastropod with a high dispersal potential. We also provide a recent literature example of how mtDNA hyperdiversity may have misguided the interpretation of genetic connectivity in the crab Opecarcinus hypostegus . Results mtDNA variation surveyed throughout the NEA showed that nearly all M. neritoides specimens had haplotypes private to populations, suggesting at first glance a lack of gene flow and thus a strong population genetic differentiation. Yet, the bush-like haplotype network, though visually misleading, showed no signs of phylogeographic or other haplotype structuring. Coalescent-based gene flow estimates were high throughout the NEA, irrespective of whether or not mtDNA hyperdiversity was reduced by removing hypervariable sites. Conclusions Melarhaphe neritoides seems to be panmictic over the entire NEA, which is consistent with its long-lived pelagic larval stage. With hyperdiverse mtDNA, the apparent lack of shared haplotypes among populations does not necessarily reflect a lack of gene flow and/or population genetic differentiation by fixation of alternative haplotypes (D EST ≈ 1 does not a fortiori imply φ ST ≈ 1), but may be due to (1) a too low sampling effort to detect shared haplotypes and/or (2) a very high mutation rate that may conceal the signal of gene flow. Hyperdiverse mtDNA can be used to assess connectivity by coalescent-based methods. Yet, the combined use of φ ST and D EST can provide a reasonable inference of connectivity patterns from hyperdiverse mtDNA, too.

Against all odds: a tale of marine range expansion with maintenance of extremely high genetic diversity

“…On the other hand, both G' ST and D, because they measure differentiation as the fraction of a deme's population that consists of private or near-private alleles 45 , will always be significantly different from zero. The hypervariable mtDNA in D. bellottii leads to a lack of shared haplotypes (with rare exceptions) among locations ( Supplementary Table S1), but this does not necessarily reflect population genetic differentiation by fixation of alternative haplotypes as previously reported by 46 . This result may be explained by a single or a combination of small sampling sizes and very high mutation rates.…”

“…for groupers 51 ). This mitochondrial region is a marker of choice in phylogeographic and connectivity studies (but on the use of hyperdiverse mtDNA for population differentiation see 46 ). The gastropod Melarhaphe neritoides revealed hypervariable mitochondrial DNA markers (16S, COI and Cytb) as a consequence of high mutation rates 49 .…”

Range‐wide phylogeography and taxonomy of the marine rock pools dwellerTigriopus fulvus(Fischer, 1860) (Copepoda, Harpacticoida)

“…The strong geographically based structuring of the genetic diversity of the Tigriopus populations inhabiting the Atlantic–Mediterranean area, which is detectable even at very small geographic scale, is possibly compatible with the long‐term persistence of Tigriopus metapopulations inhabiting isolate rocky outcrops (Burton, 1997), and the realization of dedicated studies aimed at studying the extinction and recolonization patterns of Tigriopus populations inhabiting individual pools is highly desirable. Moreover, Fourdrilis and Backeljau (2019) recently proposed that the astonishingly high genetic diversity observed in another supratidal invertebrate, the gastropod Melarhaphe neritoides (Linnaeus, 1758), could be ascribed to the occurrence of very high mutation rates, that may conceal the signal of the gene flow possibly occurring; this phenomenon is called “hyperdiversity” by Fourdrilis and Backeljau (2019). Considering our datasets, we cannot rule out that a hyperdiversity phenomenon is actually in place for Tigriopus fulvus , possibly acting synergically with other processes.…”

Genetic Polymorphism Analysis of Mitochondrial DNA from Chinese Guangdong Liannan Yao ethnic group

“…The researchers draft a phylogenetic tree of human mtDNA sequences referring to mutations of related genomes in mtDNA, and classi ed them into different haplotypes and haplogroups. Migration history of maternal ancestors of modern populations can be deduced by exploring the distribution of mtDNA haplogroups of different nationalities in different regions of the world [11][12][13] . The haplogroups named after letters composed the human mtDNA phylogenetic tree, the root of the tree represented the common maternal ancestry of all humans, which was recorded as "*".…”