Cintia P. Souto

Effects of population disjunction on isozyme variation in the widespread Pilgerodendron uviferum

Geographical range is considered a good predictor of the levels of isozyme variation in plants. Widespread species, often consisting of historically larger and more continuous populations, maintain higher polymorphism and are less affected by drift, which tends to erode genetic variation in more geographically restricted species. However, widespread species occurring in small and disjunct populations may not fit this pattern. In this study we examined genetic variation in Pilgerodendron uviferum, a conifer endemic to temperate forests of southern South America, and is such a widespread and habitat-restricted species. Twenty populations along the whole range of Pilgerodendron were analysed by isozyme electrophoresis to resolve 14 putative genetic loci. Eleven were polymorphic in at least one population although only six of them were polymorphic in more than one population. We found reduced within-population levels of isozyme variation, with only 11% polymorphic loci (0.95 criterion), 1.2 mean number of alleles per locus, and mean observed and expected heterozygosities of 0.024 and 0.033, respectively. Most genetic diversity was found within populations (HT=0.039, HS=0.033, FST 15%). Greater polymorphism and lower divergence was estimated in the more geographically restricted and closely related Fitzroya. Thus, total range, in combination with information on the degree of among-population isolation, may be a better predictor of the levels of polymorphism than range size alone.

Complex bioclimatic and soil gradients shape leaf trait variation in Embothrium coccineum (Proteaceae) among austral forests in Patagonia

Los patrones de variacion de un rasgo pueden ser adaptativos cuando varian en relacion a un gradiente ambiental. En particular, los caracteres foliares pueden afectar la productividad y la habilidad competitiva de las plantas. Identificamos patrones de variacion en el tamano y forma de la hoja con la heterogeneidad ambiental en una de las especies de mas amplia distribucion del bosque templado de Sudamerica: Embothrium coccineum (Proteaceae). Colectamos hojas y muestras compuestas de suelo de 35 poblaciones entre los 38° y 55° de latitud S, cubriendo un amplio rango de precipitacion media anual (MAP) y de temperatura media anual (MAT). En cada localidad se midieron nueve caracteres morfologicos foliares, algunos de los cuales estan correlacionados entre si, de manera que enfocaremos en algunos rasgos representativos. Predecimos que el area de la hoja (LA), el peso seco (DM), y el area foliar especifica (SLA) tenderan a aumentar y la forma de la hoja se alargara con el aumento de la temperatura, la precipitacion y la disponibilidad de nutrientes en el suelo. Tambien esperamos que el clima de la estacion de crecimiento este mas asociado con los rasgos foliares que las metricas climaticas anuales. Utilizamos regresiones multiples bivariadas y paso a paso reversas para analizar la dependencia de los rasgos morfologicos con el clima y el suelo. LA y DM aumentan con la precipitacion de verano o la temperatura del invierno, en concordancia con lo predicho. Opuesto a nuestra prediccion, LA y DM disminuyen con el aumento de la temperatura de verano, sugiriendo que en terminos de tamano foliar, E. coccineum podria percibir las condiciones climaticas del verano como un gradiente de estres que incrementa la aridez. Sorprendentemente, el SLA mostro una respuesta opuesta, aumenta con los veranos mas calurosos o secos. El indice de forma medido a traves del factor de forma (SF) se relaciona positivamente con MAT y negativamente con MAP, sugiriendo que bajo las condiciones climaticas estables del oeste de la distribucion de E. coccineum, sus hojas tienden a ser alargadas. LA y DM aumentaron positivamente con el carbono organico y fosforo disponible en el suelo, y con el nitrogeno y los cationes intercambiables, negativamente. El patron opuesto se observo para SLA. Las variables climaticas biologicamente importantes y la disponibilidad de nutrientes en el suelo son utiles para predecir el tamano y estructura de la hoja de E. coccineum. Los patrones observados en SLA podrian deberse a valores bajos de esta variable en hojas que perduran mas tiempo en la planta, que sumado al aumento del nitrogeno del suelo resulta en hojas mas esclerofilas con el aumento de la latitud. Alternativamente, podrian ser consecuencia de la relacion no isometrica entre LA y DM, de modo que hojas mas grandes, como las que ocurren en los climas con influencia oceanica hacia el oeste, tienden a tener menor SLA. Los patrones de variacion en multiples rasgos foliares a lo largo de gradientes ambientales complejos pueden no concordar entre ellos, difiriendo de lo sugerido en la literatura para rasgos que varian a lo largo de gradientes ambientales simples.

Genetic variation in the widespread Embothrium coccineum (Proteaceae) endemic to Patagonia: effects of phylogeny and historical events

Allozyme electrophoresis was used to measure and compare, with other members of the Proteaceae, levels and distribution of genetic diversity in Embothrium coccineum J.R.Forst., a widespread outcrossing species endemic of Andean Patagonian forests. We analysed variation at the species level by sampling 34 populations along its entire range of ∼20 ◦ latitude. We tested the hypothesis of multiple Pleistocene refugia by phylogeographic methods. We resolved 16 isozyme loci assayed in 934 adult trees. At the species level, total genetic diversity (HT = 0.220) was similar to that of other outcrossed and widespread plant species. Genetic parameters (NA, PSS, HE) were not statistically different from other outcrossed but mostly range-restricted Proteaceae, reflecting a strong phylogenetic imprinting for species sharing life-history traits. Populations are genetically divergent among each other (FST = 0.202). The low correlation between geographic and genetic distances suggests separate histories, i.e. multiple glacial refugia for the cold-tolerant E. coccineum. Phylogeographic trees produced different topologies, although maximum likelihood and parsimony trees shared some elements. Both trees suggest a northern and central clade, and then a separate southern clade. Current processes such as gene flow and selection confound the historic signal. These results seem in contrast to many of the northern hemisphere post-glacial phylogeographic reconstructions which show clear historical tracks of northern range expansion from southern refugia. The present study highlights the importance of phylogenetic imprinting, life-history traits and historical events driving genetic diversity patterns in this widespread Proteaceae from southern South America.

Multiple Pleistocene refugia in the widespread Patagonian tree Embothrium coccineum (Proteaceae)

Embothrium coccineum J.R.Forst. & G.Forst is an endemic tree of the Patagonian temperate forest. The objective of this study is to evaluate the impact of last glaciation events on the genetic structure of this widespread and ecologically tolerant species, to postulate possible refugial areas. Phylogeographic analyses were performed using chloroplast DNA sequences (trnL-trnF spacer and ndhC-trnV spacer) from individuals collected in 34 populations along the total range of the species, and these results were compared with a similar study in Nothofagus. A total of 22 haplotypes were found, three of which were widely distributed while 13 were found at only one location. Historical demography suggests a long period of stable effective population size, decreasing gradually towards the Last Glacial Maximum (LGM), followed by an increase in population size that stabilised 2500 years ago. The phylogeographic analyses reflect recent events of colonisation after the LGM from multiple refugia. In the northern area of its distribution probably the species survived in several pockets within the Andes mountain range and in Cordillera de la Costa in Chile. In the south, it is suggested that Embothrium survived the glacial period at the edge of the glaciers. These findings are in agreement with the fossil pollen record that shows 10 000-year-old grains in the south, suggesting colonisation from nearby areas when ice retreated. Embothrium is a coloniser that naturally occurs as scattered individuals within mixed forests. Hence, the shallow phylogeographic structure reported here reflects a Pleistocene signature highly impacted by drift resulting in the randomly fixation of new variants reducing the cpDNA structure.

Lowland valleys shelter the ancient conifer Fitzroya cupressoides in the Central Depression of southern Chile

Abstract The location of glacial refugia of tree taxa in Patagonia is determined primarily using data from the fossil pollen record. These data suggest that cold‐tolerant conifers such as Fitzroya cupressoides probably survived the Last Glacial Maximum in coastal areas of southern Chile, where vegetation types corresponded to those currently found at relatively high altitudes in the Chilean Coastal Range. Much of this region is thought to have been covered by ice. However, the question remains whether F. cupressoides could have persisted locally in ice‐free areas within the Central Depression of Chile. In this area, the species has been almost eliminated by human activities that have occurred since the 16th century. Geographic patterns of isozyme variation within 21 populations of F. cupressoides indicated that lowland populations showed high within‐population isozyme variation. In addition, lowland populations were clearly differentiated genetically from those on the coast or in the Andes. These results strongly suggest that populations of F. cupressoides persisted in the Central Depression throughout glacial times. This implies that ice caps in the south‐western Andes were probably not continuous, but, instead, the existence of ice‐free areas in lowland valleys allowed the local survival of cold‐temperate woody taxa.

How do cold‐sensitive species endure ice ages? Phylogeographic and paleodistribution models of postglacial range expansion of the mesothermic drought‐tolerant conifer Austrocedrus chilensis

In view of global climate change, it is important to understand the responses of tree species to climate changes in the past. Combinations of phylogeographic analysis of genetic evidence, coupled with species distribution models (SDMs), are improving our understanding on this subject. We combined SDMs and microsatellite data from populations of the entire range of Austrocedrus chilensis, a dominant mesotherm (cold-sensitive) conifer of dryland forests of the southern Andes, to test the hypothesis of long-distance postglacial migration from northern and warmer refugia at the Last Glacial Maximum (LGM). The SDM indicated suitable conditions for Austrocedrus in northern Chile (western) at the LGM and largely unsuitable conditions in Argentina (eastern). Population genetic diversity and effective population sizes within populations decreased southward along the Andes, consistent with the hypothesis of long-distance dispersal from a northern refugium. Results support the hypothesis of one (or a few) warmer (low latitude) refugia in Chile for Austrocedrus. On balance, the evidence suggests that in contrast to cold-tolerant tree taxa with the capacity to fast-track postglacial warming thanks to local refugia, cold-sensitive species might have undergone long-distance range expansion, lagging behind progressive climate change throughout the Holocene.

Identifying Genetic Hotspots by Mapping Molecular Diversity of Widespread Trees: When Commonness Matters

Conservation planning requires setting priorities at the same spatial scale at which decision-making processes are undertaken considering all levels of biodiversity, but current methods for identifying biodiversity hotspots ignore its genetic component. We developed a fine-scale approach based on the definition of genetic hotspots, which have high genetic diversity and unique variants that represent their evolutionary potential and evolutionary novelties. Our hypothesis is that wide-ranging taxa with similar ecological tolerances, yet of phylogenetically independent lineages, have been and currently are shaped by ecological and evolutionary forces that result in geographically concordant genetic patterns. We mapped previously published genetic diversity and unique variants of biparentally inherited markers and chloroplast sequences for 9 species from 188 and 275 populations, respectively, of the 4 woody dominant families of the austral temperate forest, an area considered a biodiversity hotspot. Spatial distribution patterns of genetic polymorphisms differed among taxa according to their ecological tolerances. Eight genetic hotspots were detected and we recommend conservation actions for some in the southern Coastal Range in Chile. Existing spatially explicit genetic data from multiple populations and species can help to identify biodiversity hotspots and guide conservation actions to establish science-based protected areas that will preserve the evolutionary potential of key habitats and species.

Correlated morphological and genetic patterns in Embothrium coccineum (Proteaceae) across climate and geography: can Embothrium survive patagonian climate change?

Adaptive radiation and reproductive isolation can determine the biogeographic structure of any species. We examine patterns of biotic variation in Embothrium coccineum, a Proteaceae tree that spans 20° of latitude and is both morphologically and genetically highly variable. We aim to (1) explore the correspondence between these biotic patterns and current geographic and climatic gradients, and (2) determine whether and how those patterns are likely to respond to changing climate. We conducted separate principal component analyses on biotic and abiotic sets of variables for 34 populations of Embothrium coccineum, accounting for a large fraction of the total variation in each. We then used canonical correlation analyses to optimise the match of those gradients onto each other. Smaller, rounder leaves and particular alleles typify the colder and drier parts of the range, whereas larger, lanceolate leaves and other alleles typify warmer and moister areas. Finally, we mapped biotic profiles onto a predicted climatic landscape, on the basis of doubling of CO2 projections. The climatic regime is predicted to shift geographically, but this lineage has successfully responded to repeated and dramatic climatic shifts since the Oligocene, and it should also be able to move and adapt quickly enough to meet the present challenge. More generally, our analytic approach can be extended to analysis of biotic and abiotic patterns in other species facing climatic challenges. Where there is enough biogeographic variation to provide adaptively relevant substrate, and where propagule dispersal is sufficiently extensive to keep up with the pace of spatial climatic shift, such taxa should be able to cope with shifting climate.

Patterns of genetic variation in tree species and their implications for conservation

Increasing concern surrounding the loss of natural forests and the decline in biodiversity has lead to a rise in research and policy initiatives in recent years. However, interest has focused primarily on lowland tropical rainforests. Tropical montane and temperate rainforests, which face similar pressures from human activities and play major roles in the livelihood of rural communities, are often ignored. Biodiversity Loss and Conservation in Fragmented Forest Landscapes is the product of over ten years of intensive field research into the changing montane and temperate rainforests of Mexico and South America. By concentrating on these largely overlooked environments, the studies reported allow for comparative analysis across areas and help identify how human disturbance has impacted the biodiversity of all forest types. Chapters incorporate features of landscape ecology, floristic biodiversity, conservation and policy and vary from in-depth investigations of a single study area to integrated examinations across regions.

Native species as goods

We thank Tassin and Kull (2015) for their response to our article on human use of non-native species (Speziale et al. 2014), which we hoped would generate discussion. We are disappointed, however, that their comment does not contribute new ideas and focuses on the following topics already discussed in the literature: that non-native species may be more productive than natives, that there is a need to produce certain products all over the world, and that humans depend on non-native species. We are not saying these contentions are false; rather, our proposal goes beyond them. New strategies are needed to reduce the negative consequences of the use of non-native species (Driscoll et al. 2014). In particular, Tassin and Kull “refute [our] idea of nativism,” but nativism (a term they do not define) is not the focus of our proposal. They also contend there are “unaddressed consequence of the proposal.” In fact, we addressed each of those consequences in our article. They also believe we confound non-native and invasive species, when we clearly differentiate them and their impacts. In answering their concerns, we followed the structure of their Comment.