Rapid adaptation to controlling new microbial epibionts in the invaded range promotes invasiveness of an exotic seaweed

Abstract

Summary Rapid adaptation to novel biotic interactions and abiotic factors in introduced ranges can be critical to invasion success of both exotic terrestrial and aquatic plants. Seaweeds are extremely successful biological invaders in marine environments. Along with herbivores, foulers − ubiquitous enemies in the marine environment − have the potential to determine the success or failure of invasive seaweeds. However, research on the topic of rapid adaptation of seaweeds to biotic challenges is still in its nascent stages and rapid adaptation of seaweeds to fouling is unexplored. We tested whether the impressive invasion success of the red macroalga Gracilaria vermiculophylla may be enhanced by the rapid adaptation of chemical control (defence) of new bacterial epibionts in the invaded range. The native and invasive G. vermiculophylla populations investigated were equally well defended against currently co‐occurring bacterial epibionts isolated from their respective ranges. In contrast, the native populations were weakly defended against bacterial epibionts from the invaded range, whereas the invasive populations were weakly defended against bacterial epibionts from their native range. Apparently during the invasion process, invasive populations have adapted their control capacity to cope with the new epibionts but have lost the capacity to fend off old epibionts. Synthesis. These results provide the first evidence that a change in habitat and, thus, confrontation by new enemies, may trigger rapid defence adaptation of seaweeds, which could be necessary for invasiveness. Such adaptation dynamics as found in the current study could be also applicable to other types of host plant – enemy interaction e.g. plant root – microbe interactions, freshwater plant – fouler interactions in general and for cases of shifting plant – enemy interactions in course of climate change.

Anti‐epiphyte defences in the red seaweed Gracilaria vermiculophylla: non‐native algae are better defended than their native conspecifics

“…However, it gives the first evidence that the capacity to defend against epibionts is higher in non-native individuals than in nativeregardless of whether the epibionts originate from the native of the non-native range of G. vermiculophylla. Our findings, therefore, seemingly contradict the observations made by Saha et al (2016), who focused on seaweed-bacteria interactions and showed that non-native G. vermiculophylla are better defended against bacterial epibionts from the non-native range but, at the same time, have reduced their capacity to defend themselves against epibionts from their home range. The contradiction may be due to the use of different micro-epibionts.…”

“…Our study is the second biogeographical comparison of defence capacities against epibionts between native and non‐native populations of G. vermiculophylla (Saha et al . ), which is now invasive in many coastal areas world‐wide. However, it gives the first evidence that the capacity to defend against epibionts is higher in non‐native individuals than in native – regardless of whether the epibionts originate from the native of the non‐native range of G. vermiculophylla .…”

“…Our findings, therefore, seemingly contradict the observations made by Saha et al . (), who focused on seaweed–bacteria interactions and showed that non‐native G. vermiculophylla are better defended against bacterial epibionts from the non‐native range but, at the same time, have reduced their capacity to defend themselves against epibionts from their home range. The contradiction may be due to the use of different micro‐epibionts.…”

Combining niche shift and population genetic analyses predicts rapid phenotypic evolution during invasion

“…As with other studies that use clonal propagation (e.g., Galloway, ), the consistency in phenotypic responses across field‐collected and common‐garden thalli indicates that population‐level differences likely have a genetic basis, but does not preclude a role for environmental history, phenotypic plasticity, or both. We note that previous studies of population‐level differentiation in G. vermiculophylla phenotypes (Hammann, Wang, Boo, Aguilar‐Rosas, & Weinberger, ; Hammann et al., ; Saha, Wiese, Weinberger, & Wahl, ; Wang et al., ) assayed populations that were not within the source region and thus could not separate prior adaptation from the signal of rapid evolution during the invasion that we infer here.…”

Chemical Defence of a Seagrass against Microfoulers and Its Seasonal Dynamics

“…To quantify the antifouling activity of eelgrass surface extracts, we used the anti-bacterial-settlement bioassay described in [41] and [23]. Bacterial isolates applied in these bioassays had been isolated previously from stones of the North Sea and Baltic Sea upper subtidal and lower intertidal zones [42] and had been conserved in −80 • C. Four bacterial isolates were used in the assays. They were Alteromonas stellipolaris (strain AMAN1), Loktanella rosea (strain AFALK1), Polaribacter dokdonensis (strain ANORD1), and Bacillus aquamaris (strain AMAN10) [42].…”