Extreme difference in rate of mitochondrial and nuclear DNA evolution in a large ectotherm, Galápagos tortoises

Caccone, Adalgisa; Gentile, Gabriele; Burns, Catherine E.; Sezzi, Erminia; Bergman, Windsong; Ruelle, Morgan L.; Saltonstall, Kristin; Powell, Jeffrey R.

doi:10.1016/j.ympev.2004.02.004

Cited by 57 publications

(40 citation statements)

References 20 publications

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“…Differences in diversity between species would be a symptom of the response to Pleistocene climate cycling. This 'just-so' explanation is not only consistent with the observational data in Mandarina (and another slow-moving taxon, Galápagos tortoise, Caccone et al 2004), but also consistent with the generally high rate of mitochondrial polymorphism in pulmonate snails (Thomaz et al 1996;Davison 2006). For Mandarina, one important consideration may be that the movement of arboreal snails is in a vertical plane (i.e.…”

Section: Discussionsupporting

confidence: 80%

Contrasting response to Pleistocene climate change by ground-living and arborealMandarinasnails from the oceanic Hahajima archipelago

Davison

Chiba

2008

Phil. Trans. R. Soc. B

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While the genetic impact of Pleistocene climate change on temperate species has been well characterized, especially in Europe and North America, an effect on the diversification of species on oceanic islands has been less well studied. This is perhaps a surprising observation given the traditional and continuing contribution of island species (e.g. Darwin's finches, Partula snails, Lord Howe Island palms) to understand speciation. Here, we combine mitochondrial and microsatellite data from the ground-living and arboreal Mandarina snails of the oceanic, subtropical Hahajima archipelago (Ogasawara, colloquially 'Galápagos of the Orient') to enable a comparative approach to understand the impact of the Pleistocene glaciations on their phylogeography. Prior work suggested that several narrowly divergent, ground-living species pairs of Mandarina populations on the outlying islands, as well as the low-lying southern and central parts of Hahajima, probably underwent bottlenecks and subsequent expansions during the recent Pleistocene. Here, the most striking finding is that largely arboreal species have deeply divergent, geographically restricted mitochondrial lineages, in contrast to a census size that is at least an order of magnitude lower than ground-living snails. As populations of both types are highly polymorphic at microsatellite loci, the systematic difference at the mitochondrial locus probably indicates a contrasting effect of the Pleistocene climate cycles on the two groups. We speculate that this may have partly come about owing to a reduced efficacy of natural selection on the more greatly structured populations of arboreal snails. If so, then a prediction is that the genome of other snails, or other species with limited mobility, will show a similar response to the Pleistocene climate cycles.

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Section: Discussionsupporting

confidence: 80%

Contrasting response to Pleistocene climate change by ground-living and arborealMandarinasnails from the oceanic Hahajima archipelago

Davison

Chiba

2008

Phil. Trans. R. Soc. B

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“…A recent literature review (Engstrom et al, in press) identified 202 mitochondrial primers that span the turtle mitochondrial genome and an additional 181 microsatellite primers but primers for only 11 nuclear loci. In addition, for problems at the within/between species boundary, many of these 11 nuclear loci have been found to be largely uninformative (Caccone et al, 2004;Spinks and Shaffer, 2005).…”

Section: An Example With Turtlesmentioning

confidence: 99%

Delimiting Species in Recent Radiations

2007

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Despite considerable effort from the systematics community, delimiting species boundaries in recent radiations remains a daunting challenge. We argue that genealogical approaches, although sometimes useful, may not solve this important problem, because recently derived species often have not had sufficient time to achieve monophyly. Instead, we suggest that population genetic approaches that rely on large sets of informative markers like single nucleotide polymorphisms (SNPs) provide an alternative framework for delimiting very recently derived species. We address two major challenges in applying such markers to species delimitation: discovering markers in nonmodel systems and using them to delimit recently derived species. Using turtles as a test case, we explore the utility of a single, relatively low-coverage genomic resource as an aid in gene and marker discovery. We exploit an end-sequenced bacterial artificial chromosome (BAC) library from an individual painted turtle (Chrysemys picta) and outline a novel protocol that efficiently identifies primer pairs that amplify homologous sequences across the tree of living turtles. Preliminary data using this library to discover SNPs in Emydura macquarii, a species that diverged from C. picta approximately 210 million years ago, indicate that sequences identified from the Chrysemys BAC library provide useful SNPs even in this very distantly related taxon. Several recent methods in wide use in the population genetics literature allow one to discover potential species, or test existing species hypotheses, with SNP data and may be particularly informative for very recently derived species. As BAC and other genomic resources become increasingly available for scattered taxa across the tree of life, we are optimistic that these resources will provide abundant, inexpensive markers that will help delimit boundaries in problematic, recent species radiations.

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“…Limited levels of variation across nuclear genes are usual at the intraspecific level in turtles (Caccone et al 2004). Sequence divergences for the mtDNA-nDNA combined data set (uncorrected ''p'' distances) range from (i) 0.3% to 0.8% between IberianMorocco group and the Menorca population, (ii) 0.1-0.2% between Iberian populations and Morocco samples, and (iii) 0.0-0.1% among Iberian populations.…”

Section: Mitochondrial and Nuclear Dna Sequence Analysismentioning

confidence: 99%

Patterns of nuclear and mitochondrial DNA variation in Iberian populations of Emys orbicularis (Emydidae): conservation implications

2007

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The European pond turtle (Emys orbicularis) is threatened and in decline in several regions of its natural range, due to habitat loss combined with population fragmentation. In this work, we have focused our efforts on studying the genetic diversity and structure of Iberian populations with a fine-scale sampling (254 turtles in 10 populations) and a representation from North Africa and Balearic island populations. Using both nuclear and mitochondrial markers (seven microsatellites, *1048 bp nDNA and *1500 bp mtDNA) we have carried out phylogenetic and demographic analyses. Our results show low values of genetic diversity at the mitochondrial level although our microsatellite dataset revealed relatively high levels of genetic variability with a latitudinal genetic trend decreasing from southern to northern populations. A moderate degree of genetic differentiation was estimated for Iberian populations (genetic distances, F ST values and clusters in the Bayesian analysis). The results in this study combining mtDNA and nDNA, provide the most comprehensive population genetic data for E. orbicularis in the Iberian Peninsula. Our results suggest that Iberian populations within the Iberian-Moroccan lineage should be considered as a single subspecies with five management units, and emphasize the importance of habitat management rather than population reinforcement (i.e. captive breeding and reintroduction) in this long-lived species.

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Extreme difference in rate of mitochondrial and nuclear DNA evolution in a large ectotherm, Galápagos tortoises

Cited by 57 publications

References 20 publications

Contrasting response to Pleistocene climate change by ground-living and arborealMandarinasnails from the oceanic Hahajima archipelago

Contrasting response to Pleistocene climate change by ground-living and arborealMandarinasnails from the oceanic Hahajima archipelago

Delimiting Species in Recent Radiations

Patterns of nuclear and mitochondrial DNA variation in Iberian populations of Emys orbicularis (Emydidae): conservation implications

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