Glacial survival, phylogeography, and a comparison of microsatellite evolution models for resolving population structure in two species of dwarf yams (Borderea, Dioscoreaceae) endemic to the central Pyrenees

Abstract

Background: Borderea is a relict genus in the Pyrenees comprising only two extant allopolyploid species. The prePyrenean, cliff-dweller B. chouardii is confined to a single critically endangered population, whereas the subalpine B. pyrenaica is more widely distributed in the mobile scree-habitats of the central Pyrenees and pre-Pyrenees. Aims: To determine the genetic structure and relationships among individuals and populations of both taxa to understand their origin. To compare two alternative evolutionary models, the Infinite Allele Model (IAM) and the Stepwise Mutation Model (SMM), in an examination of the primary factors responsible for population divergence during the Quaternary. Methods: A survey of nuclear microsatellite (Simple Sequence Repeat, SSR) variation was conducted to infer relationships among allelic phenotypes and genotypes and to evaluate the relative contributions of migration and mutation to population genetic structure. Results: The occurrence of shared ancestral alleles among populations of both Borderea species supported a presumably late-Tertiary divergence of the species in the low-altitudinal pre-Pyrenees. Borderea chouardii exhibited strong genetic differentiation between two sub-populations separated by only 150 m of vertical distance. In B. pyrenaica, populations from the pre-Pyrenees and southern Pyrenees showed greater genetic differentiation and more allelic diversity relative to populations from the northern Pyrenees. Conclusions: These results suggest that B. pyrenaica experienced glacial survival in warm southern pre-Pyrenean refugia followed by rapid postglacial migration towards the northern Pyrenees. Despite the a priori high suitability of the SMM for microsatellite markers, genotypic relationships among individuals and populations and genotypic assignments to predefined groups of B. pyrenaica were always better resolved by the IAM than by the SMM. This points towards the overwhelming influence of migration and genetic drift over mutation in the Quaternary history of the B. pyrenaica populations. However, for B. chouardii a similar pattern was shown by both evolutionary models, suggesting that sub-population divergence of this species could have also been favoured by mutation.

Challenges in analysis and interpretation of microsatellite data for population genetic studies

“…All parameters, such as the F ST ‐estimator θ (Weir and Cockerham ; Weir and Hill ), G ST , G’ ST , R ST , and D should be reported to facilitate additional interpretation and meta‐analysis (Heller and Siegismund ). However, due to their properties, indices such as F ST , R ST , and D can be useful for complementary analyses (Balloux and Lugon‐Moulin ; Segarra‐Moragues and Catalán ; Song et al. ; Whitlock ; Leng and Zhang ).…”

Morphometric and molecular variation in concert: taxonomy and genetics of the reticulate Pyrenean and Iberian alpine spiny fescues (Festuca eskiacomplex, Poaceae)

“…These altitudinal zones were recurrently covered by ice during successive glacial phases and then recolonized by founders from putative lowland, peripheral or nunatak refugia in the interglacial phases (Hewitt, ; Holderegger & Thiel‐Egenter, ). This would explain the recent divergence detected among recently established subalpine and alpine populations of some endemic Pyrenean plants, as opposed to the long isolation and large divergence observed in their closely related Pre‐Pyrenean mountain populations (Segarra‐Moragues & Catalán, ). Broad landscape genetic studies of alpine and subalpine plants conducted in the Alps and the Carpathians have concluded that species diversity is not necessarily connected with genetic diversity, pointing to the cumulative effects of availability and distribution of isolated source refugia and the adaptive success of the colonizers as the main drivers shaping the current genetic composition of the floristic diversity (Thiel‐Egenter et al ., ).…”

Genomic, spatial and morphometric data for discrimination of four species in the Mediterranean Tamus clade of yams (Dioscorea, Dioscoreaceae)

“…S5). Two narrowly endemic species of the Borderea clade survived in refugia in the Pyrenean mountains: D. chouardii, a critically endangered species with only one known locality (Goñi Martínez and Guzmán Otano, 2013), and D. pyrenaica, with a slightly wider distribution in the central Pyrenees and Pre-Pyrenees (Segarra and Catalán, 2005;Catalán et al, 2006;Segarra-Moragues and Catalán, 2008;García et al, 2012). A previous study (Viruel et al, 2016) estimated a split between these two species during the early Pliocene (~4.3 MY), whereas our results indicated that this divergence likely occurred during the late Miocene (8.1-10.6 MY).…”