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Robles in Lagunas De Epulauquen, Argentina: Previous and Recent Azpilicueta et al. Revista Chilena de Historia Natural 2014, 87:24 http://www.revchilhistnat.com/content/87/1/24 REVIEW Open Access Robles in Lagunas de Epulauquen, Argentina: previous and recent evidence of their distinctive character María M Azpilicueta1*, Mario J Pastorino1,2, Javier Puntieri2,3, Fernando Barbero1,2, Alejandro Martinez-Meier1, Paula Marchelli1,2 and Leonardo A Gallo1 Abstract The northernmost ‘robles’ of Argentina, located in Lagunas de Epulauquen (northwest Patagonia), are considered a population of Nothofagus obliqua, even though they differ in some respects from individuals of other populations of the species. In order to analyse a possible genetic basis of their distinctive character, we revised previous information and added new evidence based on biochemical (isozyme) and molecular (chloroplast DNA and nuclear microsatellite) markers, as well as quantitative trait variation (seed traits, leaf morphology, plant architecture and field performance). The comparison of Lagunas de Epulauquen specimens with specimens from other areas in Argentina demonstrated their genetic distinction. Glacial history, in conjunction with hybridisation processes, provides support for the main hypothesis to explain these results. Future research lines are proposed, aimed at identifying the taxonomic status of the Lagunas de Epulauquen population. The conservation value of these forests is highlighted. Keywords: Nothofagus obliqua; Taxonomy; Patagonia; Glacial history; Interspecific hybridisation Resumen Los robles más septentrionales de la Argentina, ubicados en Lagunas de Epulauquen (noroeste de Patagonia) son considerados una población de la especie Nothofagus obliqua, pero presentan características diferenciales respecto al resto de las poblaciones argentinas de esa especie. El presente trabajo reúne información generada previamente y otra original que demuestra el carácter genéticamente distintivo de esa población. Se presentan los resultados logrados a través de análisis genéticos con marcadores bioquímicos (isoenzimas) y moleculares (de ADN de cloroplasto y marcadores de microsatélites nucleares), con caracteres cuantitativos seminales, de morfología foliar, de arquitectura de las plantas y de aptitud a campo. La historia glacial de la región, en conjunción con procesos de hibridación pasados, se postula como la causa de esta diferenciación. Se propone la realización de nuevas líneas de investigación que permitan confirmar o re-definir el estatus taxonómico de los árboles de esta población. Adicionalmente se presenta una breve consideración sobre el valor de conservación de los bosques en Lagunas de Epulauquen, en relación a los resultados aquí presentados. Palabras clave: Nothofagus obliqua; Taxonomía; Patagonia; Historia glacial; Hibridación interespecífica * Correspondence: [email protected] 1INTA (Instituto Nacional de Tecnología Agropecuaria), EEA Bariloche, Modesta Victoria 4450, 8400 Bariloche, Argentina Full list of author information is available at the end of the article © 2014 Azpilicueta et al.; licensee Springer. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. Azpilicueta et al. Revista Chilena de Historia Natural 2014, 87:24 Page 2 of 12 http://www.revchilhistnat.com/content/87/1/24 Review separated by mountain chains, which contribute to the Nothofagus obliqua characteristics geographical isolation of Lagunas de Epulauquen. Nothofagus obliqua (Mirb.) Oerst. (Nothofagaceae, Hill Roble trees from Lagunas de Epulauquen differed from and Jordan 1993), known as ‘roble’, ‘pellín’, ‘roble pellín’ N. obliqua trees from other Argentinean populations in or ‘hualle’, is a tree species endemic to South American leaf size and margin, as well as in branching intensity temperate forests. It belongs to the Lophozonia sub-genus (Figure 2). To an even greater extent, the bud shape [recently upgraded to genus in the classification by (Figure 3A,B) and cotyledon size (Figure 4) of nursery- Heenan and Smissen (2013)] along with other six species grown seedlings from Lagunas de Epulauquen were also (Hill and Read 1991; Martin and Dowd 1993; Heenan and different to those from other Argentinean populations Smissen 2013), three of which are also South American: of N. obliqua. These observations cast doubts on the ac- Nothofagus alpina (= N. nervosa)(Poepp.&Endl.)Oerst., cepted taxonomic status of the roble population of Lagunas Nothofagus glauca (Phil.) Krasser (Veblen et al. 1996) and de Epulauquen. Nothofagus macrocarpa (A. DC.) F. M. Vázquez and R. The main goal of this study is to review previous re- Rodr. (Vázquez and Rodríguez 1999). sults and present new evidence - based on biochemical, N. obliqua is a wind-pollinated, outcrossing, anemo- molecular, morphological and architectural data - in chorous and deciduous forest tree occupying an extensive order to postulate the hypothesis that the origin of the area of 1.2 million hectares in Chile (Veblen et al. 1996; Lagunas de Epulauquen roble population is different to Araya and Oyarzún 2000). It has a narrow distribu- that of other Argentinean populations of N. obliqua. tion of 33,859 ha in Argentina, from 36° 49′ S to 40° 11′ S (Sabatier et al. 2011) along five lake basins Previous evidence supporting the distinctiveness of (Lácar, Quillén, Ñorquinco, Moquehue and Lagunas robles from Lagunas de Epulauquen de Epulauquen) and a river margin (Aluminé river; In Chile, N. obliqua forests grow approximately 50 km Gallo et al. 2000; Sabatier et al. 2011; Figure 1). The west of the Lagunas de Epulauquen population, with high distribution pattern of these forests has been markedly mountains in between. Based on pollen fossil analysis, modelled by glacial processes that affected northern Markgraf (1987) postulated the occurrence of a post- Patagonia. Palynological and palaeo-climatic studies glacial introgression within the Lagunas de Epulauquen described a non-continuous ice cap at these latitudes region, coming from the west. Therefore, a historical con- (Rabassa and Clapperton 1990). Accordingly, many species nection between the two sides of the Andes Mountains at could have survived in multiple glacial refugia (Markgraf this latitude can be inferred. et al. 1995; Veit and Garleff 1995) and gone on to re- Because of its maternal inheritance in the majority of colonise the area in post-glacial times. Genetic studies angiosperm species (Harris and Ingram 1991), chloroplast in N. obliqua forests (Azpilicueta et al. 2009) and other DNA allows direct estimation of seed-mediated dispersal. South American temperate tree species (e.g. Marchelli et al. Furthermore, the low mutation rate of the chloroplast 1998; Premoli et al. 2000; Bekessy et al. 2002; Pastorino and (Wolfe et al. 1987), which determines its highly conserva- Gallo 2002; Allnut et al. 2003; Azpilicueta et al. 2009; tive nature, helps in the inference of glacial refugia and Marchelli et al. 2010) give support to this multiple refugia post-glacial migration routes of glaciation-affected species. hypothesis. Azpilicueta et al. (2009) identified two different cpDNA Natural hybridisation is common among species of the haplotypes in the Lagunas de Epulauquen population. Nothofagus genus. N. obliqua hybridises with N. alpina, One of these haplotypes was found in two Chilean especially in sympatric forests (Donoso et al. 1990; Gallo populations from similar latitudes (Altos de Vilches at et al. 1997; Marchelli and Gallo 2000; Gallo 2004). In 35° 34′ S and Embalse Bulilleo at 36° 22′ S), support- addition, N. × leonii Espinosa (Donoso and Landrum 1979; ing the connection postulated by Markgraf (1987). The Grant and Clement 2004) is recognised as the hybrid other cpDNA haplotype found at Lagunas de Epulau- between N. obliqua and N. glauca. Finally, hybridisation quen was fixed in all the Argentinean populations of between N. obliqua and N. macrocarpa has been sug- N. obliqua growing north of Lanin volcano (39° 30′ S) gested (Vázquez and Rodríguez 1999). (Azpilicueta et al. 2009). The occurrence of natural hybridisation between Robles from Lagunas de Epulauquen N. obliqua and other congener species (see N. obliqua, Forests in Lagunas de Epulauquen, growing at 36° 49′ S, previous section) suggested a possible hybrid origin for 71° 04′ W and 1,500 masl, in an area of 1,501 ha Lagunas de Epulauquen individuals, and their identifica- (Sabatier et al. 2011), are considered the northernmost tion as possible N. × leonii hybrids was even proposed distribution of N. obliqua in Argentina. The nearest co- (Gallo et al. 2000). The proximity of potentially hybri- specific Argentinean forests are located at a distance of dising Nothofagus forests in the west (Chile) reinforced 220 km, at Moquehue lake (Sabatier et al. 2011), and are this hypothesis. N. obliqua,togetherwithN. glauca Azpilicueta et al. Revista Chilena de Historia Natural 2014, 87:24 Page 3 of 12 http://www.revchilhistnat.com/content/87/1/24 Figure 1 Distribution of Nothofagus obliqua forests in Argentina showing isohyets and sampled populations (Table 2) (from Sabatier et al. 2011). (Donoso and Landrum 1979; San Martín and Donoso frequency for Adh-2 allele - up to then considered as 1995; Le-Quesne and Sandoval 2001), N. alpina and N. species-specific for N. alpina (Gallo et al. 1997; Marchelli macrocarpa (Vázquez and Rodríguez 1999), grow in
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