Gene flow effects on populations inhabiting marginal areas: Origin matters

Abstract

The evolutionary potential of populations inhabiting marginal areas has been extensively debated and directly affects their conservation value. Gene flow is one of the main factors influencing selection, adaptive potential and thus, local adaptation processes in marginal areas. The effects of differential gene flow provenance are still not well understood, since studies on gene flow between marginal populations have been underrepresented in the literature. This kind of gene flow can be especially beneficial because it can provide both adaptive allelic combinations originated under similar environmental conditions and genetic variation on which selection can act. We conducted a study on the effects of different gene flow provenance on marginal populations of Mediterranean alpine Silene ciliata Pourret (Caryophyllaceae) replicated in three mountain ranges of Central Spain. The delineation of optimal and marginal areas of the species distribution was based on environmental differentiation and relied on the ecological definition of centrality and marginality. We experimentally tested the effect of three different types of pollen‐mediated gene flow on germination rate, seedling size and survival rate in marginal populations and assessed their effects by establishing in situ common gardens. To further assess the evolutionary potential of marginal populations, we performed a reciprocal sowing experiment and measured the same fitness components to determine the extent of local adaptation. We found that gene flow between marginal populations improved germination rate and seedling survival with regard to gene flow from optimal to marginal populations and within marginal populations. In reciprocal sowing experiments, seedling survival rate was higher when the seed source was from marginal areas than when it was from optimal areas in both marginal and optimal sowing sites. Synthesis. Our results suggest that gene flow between marginal populations from similar environmental conditions increases the fitness of the recipient population by increasing genetic diversity and simultaneously providing adaptive alleles generated under similar selective pressures. Results also highlight the adaptive potential of marginal populations as genetic diversity from marginal areas may provide a fitness advantage to the populations in optimal areas. In this context, the adaptive value of marginal populations increases their relevance and potential use in conservation management.

Evaluating Assisted Gene Flow in Marginal Populations of a High Mountain Species

“…The experimental gene flow design was not reciprocal as it was focused on studying the effects of assisted gene flow on the marginal populations occurring at the low elevation distribution edge. Thus, the recipients of gene flow treatment were always the marginal populations as in previous study assessing similar questions (see Morente-López et al, 2020a).…”

“…However, gene flow effects on the adaptive potential of recipient populations are closely related to the specific environmental conditions of the original and recipient populations. In this sense, Morente-López et al (2020a) showed that gene flow between marginal populations that share similar environmental conditions increase genetic diversity and provide adaptive alleles. Other studies point to a reduction of fitness in marginal populations due to the incorporation of maladapted alleles from optimal populations (Dawson et al, 2010;Fedorka et al, 2012).…”

“…In essence, the potential pros and cons of assisted gene flow have yet to be ground-proved in natural populations under contrasting situations to gain insight on the applicability of this approach. Also, it is important to measure the effects of gene flow on different traits throughout the ontogeny and assess whether the same gene flow can produce contrasting fitness effects on different life stages (Angert et al, 2008;Morente-López et al, 2020a). This is crucial because the outcome of a conservation action would depend on the overall response of the different fitness components measured.…”

Áreas marginales en ecosistemas alpinos: definición y valor evolutivo en un contexto de cambio climático

“…A pesar de los niveles sustanciales de flujo genético encontrados entre poblaciones, todavía existen algunos niveles de aislamiento que generan una estructura genética y, en consecuencia, puede existir diferenciación fenotípica asociada a procesos neutrales como la deriva genética, los cuellos de botella o efectos fundadores. En uno de los pocos estudios realizados para testar el efecto diferencial del flujo genético con respecto a su origen, encontramos que la supervivencia de las plántulas resultantes del flujo genético entre poblaciones marginales fue mayor que la de plántulas resultantes del flujo genético de poblaciones óptimas a poblaciones marginales (Morente-López et al 2020b). Ambas son etapas vitales cruciales para la especie ya que su mayor cuello de botella demográfico se encuentra en la fase de reclutamiento (Giménez-Benavides et al 2008;Giménez-Benavides et al 2011b).…”

“…En este contexto, los resultados de los experimentos de siembra cruzada realizados con S. ciliata mostraron una mayor tasa de supervivencia de las plántulas procedentes de poblaciones marginales, tanto cuando eran sembradas en áreas óptimas como en áreas marginales. Esto indica una mayor capacidad de adaptación de las poblaciones marginales que de las poblaciones óptimas a las condiciones ambientales existentes en las fases de germinación y establecimiento (Morente-López et al 2020b). Este hallazgo asegura y refuerza el potencial adaptativo presente en poblaciones marginales expuesto en puntos anteriores basado en la diversidad genética presente y la capacidad de las poblaciones de divergir fenotípicamente en respuesta a unas presiones selectivas dadas (García-Fernández et al 2012a;Lara-Romero et al 2016a;Morente-López et al 2018).…”