Abstract The effect of environmental gradients on the remarkable diversity of mountain‐associated plants and on the species' abilities to cope with climate change transcends species‐specific ...strategies. For instance, our understanding of the impact of thermal gradients on ecological divergences in populations of widely distributed species is limited, although it could provide important insights regarding species' response to climate change. Here, we investigated whether populations of an endemic species broadly distributed across an elevation gradient employ unique or multiple divergent ecological strategies according to specific environmental conditions. We hypothesised that populations employ distinct strategies, producing a tolerance‐avoidance trade‐off related to the thermal conditions they experience across elevations. We conducted our research with 125 individuals of Pitcairnia flammea (Bromeliaceae) sampled from various elevations spanning from sea level to ~2200 m and cultivated under the same conditions. To assess specific ecological strategies of P. flammea populations across elevations, we examined leaf temperature, heat and cold tolerances, as well as other structural/morphological, optical, physiological and biochemical leaf traits. We majorly observed that water‐saving traits diminish as elevation increases while membrane fluidity, majorly associated with unsaturated and very‐long‐chain lipids, enhances. Low‐elevation individuals of P. flammea invest in water storage tissues, which likely prevent excessive water loss through the intense transpiration rates under warming periods. Conversely, high‐elevation plants exhibit increased membrane fluidity, a possible response to the stiffening induced by low temperature. Our results revealed a tolerance‐avoidance trade‐off related to thermal strategies of populations distributed across an elevation gradient. Low‐elevation plants avoid excessive leaf temperature by investing in water‐saving traits to maintain transpiration rates. High‐elevation individuals, in turn, tend to invest in membrane properties to tolerate thermal variations, particularly cold events. Our findings challenge the conventional notion that plants' vulnerability to warming depends on species‐specific thermal tolerance by showing diverse thermal strategies on populations across an elevation gradient. Read the free Plain Language Summary for this article on the Journal blog.
Resumo O efeito dos gradientes ambientais na grande diversidade de plantas associadas a montanhas transcende as estratégias específicas de cada espécie. Nosso entendimento sobre o impacto dos gradientes térmicos nas divergências ecológicas em populações de espécies amplamente distribuídas, por exemplo, é limitado, embora possa fornecer informações importantes sobre a resposta das espécies às mudanças climáticas. Aqui, investigamos se populações de uma espécie endêmica e amplamente distribuída em um gradiente altitudinal, empregam estratégias ecológicas únicas ou múltiplas de acordo com condições ambientais específicas. Nossa hipótese é que as populações empregam estratégias que resultam em um equilíbrio entre tolerância e evitação relacionado às condições térmicas que experimentam em diferentes altitudes. Analisamos 125 indivíduos de Pitcairnia flammea (Bromeliaceae) amostrados em diversas altitudes, desde o nível do mar até cerca de 2.200 metros, e cultivados nas mesmas condições. Para avaliar as estratégias ecológicas específicas das populações de P. flammea , examinamos temperatura foliar, tolerâncias ao calor e ao frio, além de outros traços foliares estruturais/morfológicos, óticos, fisiológicos e bioquímicos. Vimos que características de economia de água diminuem à medida que a altitude aumenta, enquanto a fluidez da membrana, associada principalmente a lipídios insaturados e de cadeia muito longa, aumenta. Indivíduos de baixa altitude investem em tecidos de armazenamento de água, provavelmente prevenindo a perda excessiva de água durante períodos de aquecimento e com taxas intensas de transpiração. Por outro lado, plantas de altas altitudes possuem maior fluidez de membrana, uma possível resposta ao enrijecimento induzido por baixas temperaturas. Nossos resultados revelaram um equilíbrio entre tolerância e evitação relacionado às estratégias térmicas de populações distribuídas ao longo de um gradiente de altitude. Plantas de baixa altitude evitam temperaturas foliares excessivas investindo em características de economia de água para manter as taxas de transpiração. Indivíduos de alta altitude, por sua vez, tendem a investir em membranas que toleram variações térmicas, especialmente eventos frios. Nossas descobertas desafiam a noção convencional de que a vulnerabilidade das plantas ao aquecimento depende da tolerância térmica específica da espécie, mostrando estratégias térmicas diversas em populações ao longo de um gradiente de altitude.
Aim
Ancient climatic fluctuations are invoked as the main driving force that generates the astonishing biodiversity in ancient mountains. As a result, endemism and spatial turnover are usually high ...and few species are widespread amongst entire mountain ranges, precluding the understanding of origins of macroevolutionary patterns. Here, we used a species endemic to, but widespread in, one of the most species‐rich ancient mountains in the globe to test how environmental changes acted on and how their macroevolutionary patterns were shaped.
Location
Espinhaço Range, Eastern Brazil.
Taxon
Vriesea oligantha species complex (Bromeliaceae).
Methods
We compiled data for plastidial regions and nuclear microsatellites to assess genetic diversity, population structure, migration rates and phylogenetic relationships. Using temperature and precipitation variables, we modelled suitable areas for the present and the past, estimating corridors between isolated populations. We also implemented Bayesian demographic analyses to estimate ancient populations dynamics. Finally, we tested if population structure is driven by isolation by environment or by distance using a Bayesian modelling approach.
Results
Our results showed that the intraspecific divergence events of V. oligantha are older than those associated with the latest Pleistocene climatic oscillations, supporting the view that Quaternary climatic fluctuations are key components for understanding its population differentiation processes. Species distribution modelling estimated corridors between populations in the past, as also shown in the demographic analyses, depicting a major spatial reorganization during colder climates. Besides, the high genetic structure estimated results from both models of isolation by distance and by environment.
Main conclusions
V. oligantha is a remarkable model to test the effects of climatic oscillations over the biological community, since this species originated in the early‐Pleistocene, prevailing over several cycles of climatic fluctuations until today. The estimated demographic dynamics of V. oligantha agrees with the species‐pump mechanism, suggesting it as the main cause of speciation within the Espinhaço Range. Moreover, the phylogeographic patterns of V. oligantha reflect previously recognised spatial and temporal macroevolutionary patterns in the Espinhaço Range, providing insights into how microevolutionary processes may have given rise to this astonishing mountain biodiversity.
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