In our new post Pedro Gundel, researcher at University of Talca (Chile) presents his work ‘Temporal host–symbiont dynamics in community contexts: Impact of host fitness and vertical transmission efficiency on symbiosis prevalence’. He shows how symbiotic species transmit between generations, discusses the complexity of ecological processes and shares the long path that paved the way to this work.
About the paper
A major topic in biological sciences is the study of symbiotic relationships between plants and microorganisms to understand how they influence the ecology and evolution of each other. Eco-evolutionary perspectives predict that interactions between plants and maternally inherited microorganisms may promote mutualistic relationships, meaning that both partners benefit from living together. Because the presence of symbionts should enhance host fitness, these relationships are expected to reach high prevalence in host populations. However, the prevalence of symbiosis can vary, as the symbiosis outcomes are context-dependent, and vertical transmission efficiency can fluctuate. Given the eco-evolutionary framework, it is expected that the transmission process aligns with the outcomes of context-dependent symbiosis in nature.
We used the symbiosis between an annual plant species and its vertically transmitted fungal endophyte as model system. Over three consecutive years, we surveyed populations of this host plant in paired stands of two adjacent but biophysically contrasting vegetation communities in a grassland known as Flooding Pampa, in the Argentinean Pampa Region. We aimed to uncover the contribution of two major determinant processes to the prevalence of symbiosis across years and vegetation communities: (i) the effect of symbiosis on host fitness (by comparing symbiotic and non-symbiotic plants) and (ii) the vertical transmission efficiency at the individual level. In addition, we wanted to determine whether the efficiency of vertical transmission aligns with the outcomes of context-dependent symbiosis.
About the research
The study included both temporal and spatial variation, as it spanned three consecutive years and stands from two vegetation communities, respectively. We were fortunate that the years varied greatly in precipitation; one year was well below the mean annual precipitations, while another was well above it. The two vegetation communities were Humid Mesophytic Meadows, which are more productive and experience lower levels of stress, and Humid Prairies, which are less productive and experience higher levels of stress. We sampled a total of 758 plants, each individual was characterized in terms of its symbiotic status, seed production (fitness) and transmission efficiency (proportion of endophyte-bearing seeds in endophyte-symbiotic plants).
We observed intriguing dynamics in the symbiosis prevalence across the three years. Over the three years, symbiosis prevalence remained consistently high at about 100% in the Humid Mesophytic Meadows, while it was around 75% in the Humid Prairies. Interestingly, plant fitness varied considerably across years. Plants showed very low fitness in the dry year and high fitness during high-precipitation years. Notably, endophyte-symbiotic plants showed significantly better fitness in the Humid Mesophytic Meadows, particularly in years with higher precipitation.
The efficiency of endophyte vertical transmission was higher in the Humid Mesophytic Meadows (96%) than in the Humid Prairies (93%). Transmission rates remained the same over the years and did not correlate with plant fitness. Since we worked with an annual plant species that does not form a persistent soil seed back, we were able to calculate the changes in endophyte prevalence from seeds and to mature plants; this allowed us to check whether there was a selection favouring or against symbiotic plants within each growing cycles. With this approach, we observed that despite the inefficiencies in transmission within Humid Prairies, there was a fitness advantage for symbiotic plants over non-symbiotic ones.
Vertical transmission is expected to promote mutualism by aligning the fitness of both partners. Although symbiotic plants showed higher fitness and transmission failures were more frequent in low-fitness plants, variation in transmission efficiency among individual plants and across vegetation communities was not directly linked to host fitness. Our study highlights how context-dependent vertical transmission efficiency and endophyte-mediated fitness benefits interact in complex ways to shape symbiosis prevalence in populations across vegetation communities.
About the author
I am an agronomist with interest in Ecology. I have done most of my academic and scientific career at IFEVA (Institute of Agricultural Plant Physiology and Ecology), Faculty of Agronomy, University of Buenos Aires and CONICET (National Scientific and Technical Research Council). Currently, I work at the Centre of Integrative Ecology (CEI), Institute of Biological Sciences (ICB), University of Talca, Chile.
I completed my doctoral thesis at the University of Buenos Aires (School for Graduates “Alberto Soriano,” Faculty of Agronomy), Argentina, from 2004 to 2009 (A very long time ago!). My thesis focused on the controls of endophyte symbiosis prevalence in grass populations, especially focusing on the role of the transmission process. Until that time, the research on the topic had centered on studying the relative fitness of endophyte-symbiotic and non-symbiotic plants (as the main driver of symbiosis prevalence). So, we wanted to shift the focus to the transmission process, which had been largely overlooked.
My thesis combined both modelling and experimental work, using seeds and plants under controlled conditions. In a way, this current study feels like the culmination of that journey, finally going into the field and unrevealing the complex interplay between these studied processes. Seeing this research published in such a prestigious journal is a truly rewarding milestone, not just for me, but also for those who supported me along the way. So, a huge thanks to everyone!
I hope our work inspires young scientists to explore plant-endophyte symbiosis from both ecological and evolutionary perspectives.
Like this post? Read the research here.
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