The uncertainty of Late Pleistocene range expansions in the western Mediterranean: a case study of the colonization of south‐eastern Spain by the spur‐thighed tortoise, Testudo graeca

Abstract

Aim Recent biogeographical studies have postulated a North African, Late Pleistocene, origin for some species of the Iberian Peninsula. However, a robust assessment of such range expansions requires high-resolution molecular tools to resolve overlapping biogeographical and cultural processes. Here we aim to determine whether the spur-thighed tortoise, Testudo graeca, arrived in southeastern Spain during historical or prehistoric times, and whether its dispersal to the Iberian Peninsula was human-mediated.Location The western Mediterranean Basin (south-eastern Spain, northern Algeria and north-western Morocco).Methods Using 428 samples from 19 sites in North Africa and 18 in southeastern Spain, we obtained mitochondrial sequences from the cytochrome b gene and genotypes derived from seven microsatellite loci. These data were employed to obtain population genetics descriptors, haplotype networks, Bayesian cluster analyses and isolation-by-distance patterns. Moreover, we used a Bayesian demographic approach to delimit the dates involved in the range expansion.Results We found lower levels of genetic variability and weak mitochondrial differentiation in the south-eastern Spanish tortoises compared with the North African ones. However, exclusive haplotypes occurred in the Iberian samples and microsatellite cluster analyses revealed moderate levels of admixture across both sides of the Mediterranean. A coastal area in the west of Algeria and the central-southern region in south-eastern Spain are suggested as the most probable founder and arrival places, respectively. Finally, we identified signatures of an ancient bottleneck event approximately 20,000-30,000 years ago. Main conclusionsThe spur-thighed tortoise probably arrived in south-eastern Spain during Late Pleistocene sea-level low stands. The role that humans may have played as dispersers across the Mediterranean remains unclear. Our results are in accordance with other recent findings of trans-Mediterranean expansions during this period and highlight the importance of employing precise methodological approaches before a species can be considered as historically introduced.

Surfing in tortoises? Empirical signs of genetic structuring owing to range expansion

“…which the finding of an isolation-by-distance pattern suggests the natural expansion of the species within the colonized area from a single arrival point located in the central-southern part of the current range, as proposed by Graciá et al [9,10]. In this range expansion context, we find a spatially structured genetic pattern within the Spanish range that shows several signatures predicted by genetic surfing: (i) genetic diversity significantly decreases with increasing distance to the probable arrival area for the species; (ii) more clinal patterns of allele frequencies involving different unlinked loci are present in the expanded population; (iii) some of these clinal patterns correspond to African rare alleles that are frequent in some areas of southeastern Spain; and (iv) spatial differentiation is stronger in the more recently established range than in the original one.…”

“…Moreover, the finding of a spatially coherent pattern of genetic variation within the recent population supported the natural dispersal of the species within the newly colonized territory from a single point of entry located in the central-southern part of the current range [9,10].…”

“…However, for the largest population, located in southeastern Spain and only involving the subspecies Testudo graeca graeca (figure 1), an alternative possibility has been suggested. In a recent study, we found signatures of an ancient bottleneck event approximately 20 000-30 000 years ago [9].…”

“…We used five previously used polymorphic microsatellite markers (GenBank accession numbers: AF517235, AF517229, AF517239, AY822049 and AY822051; table 1), and only those samples coming from sites with at least seven individuals were included in the subsequent analyses [9,10].…”

“…In previous studies, we have described the time since colonization of Spain and the genetic differentiation within the original North African population of T. graeca [9,10]. In the current study, we explore the dispersal process of T. graeca in southeastern Spain, addressing the main predictions of the genetic surfing theory.…”