Constraining the physiological, genetic, and symbiotic adaptation of an invasive foraminifera in the Mediterranean Sea

Abstract

Global change may directly or indirectly influence biological invasions by increasing the chances of the introduction and establishment of alien species into new habitats. Such processes pose major threats to biodiversity and the resulting changes in ecosystems may have serious functional and economic impacts. A dramatic migration of tropical species from the Red Sea into the Mediterranean Sea was triggered when the Suez Canal was opened in 1869. Some invaders became highly abundant in their new locations, such as the benthic foraminifera Amphistegina lobifera. In its newly conquered Mediterranean habitat, the invasive populations are exposed to particularly low temperatures in winter (~13°C) and warmer temperatures in summer (~31°C), which represents a seasonality that exceeds the range of their native habitat (22°C in summer and 28°C in winter). This prolific calcifier that relies on photosymbiosis with diatoms has recently expanded its invasion front to Sicily and in a short period after its first appearance in 2016, the species became particularly abundant, sometimes reaching 50% of the benthic foraminifera assemblages. Therefore, to forecast future invasions and understand their impact in the new location it’s crucial to comprehend the mechanisms by which a species might become a successful invader. In this context, this thesis aims to understand if the adaptation necessary to survive in the Mediterranean were already present in the foraminifera host and symbionts from the source population in the Red Sea (niche conservatism concept) or if the invasion success was due to rapid emergence of new adaptations in the invaders (inducing ecological niche shifts). For this, several approaches are applied, including genetic population structure, metabarcoding analyses, and physiological experiments. To constrain if the invasion either induces or is facilitated by genetic adaptation of the foraminifera host or if the source population sustains key pre-adaptations to the new conditions, the population structure of A. lobifera across its invasive range was investigated (Chapter 1). The analyses revealed that the invading populations do not exhibit genetic divergence from the source population, and the invasion success in the Mediterranean Sea is associated with the combination of preadaptation, high dispersal ability, and ongoing reseeding from the Red Sea. However, given an increased genetic variation among individuals and decreased intragenomic variability, the invading populations appear to be affected by the invasion. The invasion, therefore, appears to be associated with a sustained change in reproductive strategy toward the abandonment of sexual reproduction, or with an increased failure in sexual reproduction and enhanced asexual reproduction, which could represent a long-term loss of adaptive potential. In order to resolve if the local adaptation was enhanced by beneficial microbiome associations that the foraminifera acquired during the invasion, or if they carry the same associations as the source population, metabarcoding analyses of the foraminiferal microbiome (eukaryotic and bacterial) and the surrounding environmental DNA were applied (Chapter 2). Different bacterial microbiomes and diatom sequence variants were associated with the different host populations. However, the vast majority of the diatom sequence variants were absent in the environment. This implies that the foraminifera either preserve an ancestral stock of symbionts, with new strains emerging inside the host over the invasive range, or that they acquired their symbionts along the invasive range or during different seasons. These findings show that the algal symbiosis composition is flexible, and its modification may enable the holobiont to deal with the unique temperature regime of the invaded habitat. Finally, to assess if the sustained exposure to colder winters in the invasive locations induced physiological adaptations in the foraminiferal holobiont, or if the success is a matter of a pre-adaptation inherited from the source population, a physiological experiment was performed (Chapter 3). In a four-week experiment, the physiological responses of the foraminifera host and its symbionts to colder temperatures (10, 13, 16, 19 °C + control at 25°C) were evaluated for the source, pioneer invaders, and invasion-front populations. The 13°C treatment represents the minimum temperature experienced in the invaded habitat and 10°C is an out-of-range treatment to assess whether the population has a higher adaptive range than already displayed. It was observed that the foraminifera host and its symbionts respond differently to cold stress. While there were no noticeable differences in survival and performance of the host (all populations showed low tolerance to cold temperatures < 16°C), the symbionts showed enhanced tolerance to cold temperatures (~13°C). In addition, the invasion front population symbionts were significantly resilient to even lower temperatures (10°C). Thus, the symbionts are likely the main responsible for the success of invasion under cold stress. These results advance our understanding of the mechanisms regulating the invasion of a prolific calcifier benthic foraminifera in the Mediterranean Sea. The overall results indicate that the cold-tolerant photosymbiosis or the flexibility to form symbiosis with differently adapted diatoms is likely a key to the success of past and future migrations of this species. This can be used to refine models of ecological niche shifts during invasions and improve predictions of future marine invasions.