Date Published: January 24, 2017
Publisher: Public Library of Science
Author(s): Marta Vila, Miguel Hermida, Carlos Fernández, Silvia Perea, Ignacio Doadrio, Rafaela Amaro, Eduardo San Miguel, Tzen-Yuh Chiang.
Genetic isolation and drift may imperil peripheral populations of wide-ranging species more than central ones. Therefore, information about species genetic variability and population structure is invaluable for conservation managers. The Iberian populations of three-spined stickleback lie at the southwestern periphery of the European distribution of Gasterosteus aculeatus. This teleost is a protected species in Portugal and Spain and local extinctions have been reported in both countries during the last decades. Our objectives were (i) to determine whether the Iberian populations of G. aculeatus are unique or composed of any of the major evolutionary lineages previously identified and (ii) to assess the evolutionary potential of these peripheral populations. We genotyped 478 individuals from 17 sites at 10 polymorphic microsatellite loci to evaluate the genetic variability and differentiation of the Ibero-Balearic populations. We also sequenced 1,165 bp of the mitochondrial genome in 331 of those individuals in order to complement the estimates of genetic diversity in the Ibero-Balearic region. We predicted the evolutionary potential of the different sites analysed based on the contribution of each of them to total allelic/mitochondrial diversity. An intraspecific phylogeny at European level was reconstructed using our data from the mitochondrial cytochrome b gene (755 bp) and published sequences. The so-called Transatlantic, European and Mediterranean mitochondrial lineages were found to be present in the Ibero-Balearic region. Their phylogeography suggests a history of multiple colonisations. The nuclear results show, however, a strong correlation between population structure and drainage system. The following basins should be prioritised by conservation policies in order to preserve those populations with the highest evolutionary potential: the Portuguese Vouga and Tagus as well as the Spanish Majorca and Limia. Maintenance of their connectivity, control of exotic species and monitoring of habitat properties are strongly recommended in those areas. Genetic variation alone cannot, however, ensure the persistence of these peripheral southern populations of G. aculeatus. On the one hand, the analysis of a historical sample from Eastern Spain (Penyscola) revealed no genetic erosion, which suggests a fairly sudden extinction of that population. On the other hand, the reintroduction program implemented in the Valencian Community has mostly failed despite our finding of similar level of genetic diversity between the wild source and the captive-bred released individuals.
The combined effects of isolation and drift may cause peripheral populations of wide-ranging species to be more imperilled than central ones [1, 2]. This is because low genetic variation is expected to decrease their potential for continuous adaptation . Therefore, knowledge about their genetic diversity and population structure is invaluable for conservation policy and management. However, policy-makers and managers usually need a more practical approach to apply genetic data to conservation biology . One such example is predicting and ranking the evolutionary potential of different breeds  or wild populations  by assessing their contribution to global diversity .
Contrasting with the perspective shown by mitochondrial data, G. aculeatus from the Ibero-Balearic region showed a nuclear population structure, which was highly concordant with the hydrological pattern. This pattern resembles the case of Salmo trutta from Western Mediterranean streams, where isolation between basins was enhanced by the absence of anadromous individuals in that area and the presence of barriers to migration . The analysis of conservation priorities identified Majorca, Vouga, Antela and Tagus as the populations that contribute the most to the maximal genetic diversity of Ibero-Balearic G. aculeatus.
The Transatlantic, European and Mediterranean mitochondrial lineages recognised and defined for G. aculeatus by prior literature were present in the Ibero-Balearic region. By contrast, the Black Sea, Adriatic and Irish lineages were absent. Our results suggested that Atlantic three-spined sticklebacks colonised the Iberian Peninsula several times during the end of the Last Glacial period. G. aculeatus showed a strong nuclear population structure highly concordant with the Iberian hydrological pattern. The Portuguese populations of Vouga and Tagus, as well as the Spanish Antela (Northwest Spain) and Majorca should be prioritised by conservation policies. Their loss would severely erode the genetic diversity of G. aculeatus in the Ibero-Balearic region, so maintenance of their connectivity with nearby populations, control of exotic species, and monitoring of habitat properties are recommended in those areas. We would like to highlight the conservation value of the Central and Southern Portuguese populations, not simply because of their genetic and habitat distinctiveness, but rather because of the indication of sporadic coastal dispersal involving Mira and Sado. The site of Penyscola showed an intermediate level of genetic diversity, so that its extinction was likely too abrupt to leave any genetic footprint. Lastly, the ex-situ conservation program implemented in the Valencian Community mostly failed despite ensuring a similar level of genetic diversity between the source and the captive-bred individuals. Environmental changes caused by human activity have been frequently argued to explain local declines and extinctions reported during recent decades, particularly with regard to the influence of exotic species and modification of drainage patterns caused by land-use changes. However, the persistence of peripheral populations at southern latitudes may be also conditioned by the tolerance of G. aculeatus to physiochemical changes related to global warming. Our allelic-diversity results are expected to contain information regarding the evolutionary potential for adaptation to environmental changes. Nevertheless, a deeper knowledge about the relative contribution of extrinsic and intrinsic factors to fitness is needed in order to properly undertake conservation actions that will preserve the three-spined stickleback at low latitudes.