Introduction
Among the anthropogenic processes driving the contemporary loss of
biodiversity and ecosystem functions, biological invasions play a major,
but complicated role (Hooper et al., 2012). Their consequences for
recipient ecosystems can range from devastating, to neutral, and even to
positive, but they are generally difficult to predict as the effects are
spread over multiple trophic levels (Simberloff, 2011). To become
established in a new habitat, invaders have to face harsh conditions
during transportation (e.g., unsuitable temperatures, anoxia, darkness)
followed by different and sometimes novel conditions in the non-native
environment. During and after transport such conditions may act as
selective filters that favor certain phenotypes (Bax, Williamson,
Aguero, Gonzalez, & Geeves, 2003; Blackburn et al., 2011). Compared to
non-invasive populations or species, invaders tend to be more tolerant
toward stressors (Walther et al., 2009), possess superior performance
traits (e.g., growth rate, photosynthetic rate, nitrogen use efficiency;
Van Kleunen, Weber, & Fischer, 2010), and to have higher plasticity,
which enables them to express more successful phenotypes across
different environments (Richards, Bossdorf, Muth, Gurevitch, &
Pigliucci, 2006). Moreover, invasive plants may be morepromiscuous (or flexible ) toward microbiota, which
increases the probability of acquiring the same microbial functions from
a different pool of potential symbionts available in the new environment
(Klock, Barrett, Thrall, & Harms, 2015; Maggia & Bousquet, 1994;
Rodríguez‐Echeverría, Le Roux, Crisóstomo, & Ndlovu, 2011).
Host promiscuity (Perret, Staehelin, & Broughton, 2000) has also
been termed host generalism (Rodríguez‐Echeverría et al., 2011)
or microbiome flexibility (Voolstra & Ziegler, 2020) and was
recently hypothesized to be a broadly occurring phenomenon among
holobionts, that can promote the ability of hosts to respond and
acclimate to environmental stress on short time scales (Voolstra &
Ziegler, 2020). For invasive species which are transported to different
environments, such a benefit would be particularly relevant as
promiscuous hosts would not only be able to invade environments similar
to the native environment, but would also be potentially invasive in a
wider range of environments.
Whereas invasive plants have a
major global impact terrestrially (Morales & Traveset, 2009; Pimentel,
Zuniga, & Morrison, 2005), invasive macroalgae, or seaweeds, have
caused analogous ecosystem effects in marine systems (Williams & Smith,
2007). As holobionts (see definition in Bordenstein & Theis, 2015),
macroalgae are continuously interacting with microbial organisms from
the water column, which colonize and penetrate their surfaces and
tissues (Wahl, Goecke, Labes, Dobretsov, & Weinberger, 2012). Some of
these fouling microbes may be harmless, or protective (e.g., Li et al.,
2021; Saha & Weinberger, 2019), involved in the regulation of host
morphogenesis (Spoerner, Wichard, Bachhuber, Stratmann, & Oertel, 2012)
or spore release (Weinberger et al., 2007), or facilitating the
acquisition of nitrogen and/or vitamins (Croft, Warren, & Smith, 2006;
Gerard, Dunham, & Rosenberg, 1990; Kazamia et al., 2012). Other taxa
may represent a threat as opportunistic or specialized pathogens (Egan,
Fernandes, Kumar, Gardiner, & Thomas, 2014; Egan & Gardiner, 2016;
Saha & Weinberger, 2019; Weinberger, Friedlander, & Gunkel, 1994;
Weinberger, Hoppe, & Friedlander, 1997). Macroalgae manipulate the
associated microbial community by means of chemical defense, for
instance with specialized metabolites that target microbial fouling
agents by interfering with quorum sensing (Harder, Campbell,
Egan, & Steinberg, 2012). They also produce cue metabolites to attract
and deter protective and harmful or (opportunistically) pathogenic
symbionts (Kessler, Weiss, Kuegler, Hermes, & Wichard, 2018; Saha &
Weinberger, 2019).
Recent evidence suggests that similar to plant invasions, host
promiscuity may also be important in seaweed invasions. Using the
invasive rhodophyte Gracilaria vermiculophylla (Ohmi) Papenfuss
(synomym: Agarophyton vermiculophyllum ), Bonthond et al. (2021)
conducted a common garden experiment, where native and non-native
populations were subjected to a simulated invasion, experiencing
disturbance followed by exposure to a new environment. Compared to
native hosts, the epibiota of non-native populations changed more with
respect to their epibiota in the field. The epibiota of non-native
populations also became more similar to each other, suggesting that
non-natives are indeed more promiscuous toward potential symbionts and
may therefore acclimate more easily to new conditions. The authors also
observed that epibiota associated with native holobionts dispersed more
within-populations. The two measures of beta diversity between- and
within-populations represent different characteristics of a community,
and especially in a common garden should be interpreted separately.
Whereas the beta diversity between-populations relates to the degree of
change in epibiota in response to the environment, thewithin-population beta diversity is instead related to the degree
of stress experienced by holobionts from that population. This
stress-driven increase of variability in microbiota (or dispersion
effect) is also known as the Anna Karenina Principle (Zaneveld,
McMinds, & Thurber, 2017), which predicts that microbiota disperse due
to a relative increase of stochastic processes (or relative decrease in
deterministic processes) acting on the holobiont. Therefore, the
findings in Bonthond et al. (2021) do not only suggest that non-native
hosts are more promiscuous (beta diversity is lower between non-native
populations) but may also indicate that non-native holobionts are less
susceptible to stress or have more stable communities (beta diversity is
lower within non-native populations).
Based on this idea, we aimed to specifically compare how epibiota
associated with native and non-native G. vermiculophyllapopulations disperse in response to stress. A common garden experiment,
similar to Bonthond et al. (2021), was conducted to simulate an invasion
event by disturbing G. vermiculophylla ’s prokaryote communities
with antibiotics. We also included a temperature treatment, subjecting
native and non-native holobionts to optimal and (moderately) stressful
thermal conditions. Here, we assumed that as subjects in the same common
garden are exposed to the same environment, only processes originating
from the host can vary. This implies that differences in beta diversity,
which reflect differences in the ratio of deterministic and stochastic
processes acting on the epibiota and therewith stability, originate from
the host as well and are most likely explained by an in- or decrease of
processes with which the host influences its epibiota. With two
thermally different common gardens, we extended this idea to compare
dispersion between two environments that only differed in temperature,
expecting that non-native holobionts are less susceptible to thermal
stress and therefore disperse less under stressful conditions.
Gracilaria vermiculophylla, native to the northeast Pacific, has
become a widespread, invasive species along the coasts of North America,
northwestern Africa, and Europe (see Krueger‐Hadfield et al., 2021, 2017
and references therein). The rhodophyte is known to be chemically well
equipped to manipulate microbiota (Saha & Weinberger, 2019; Saha,
Wiese, Weinberger, & Wahl, 2016), and multiple lines of evidence
suggest that the interaction between host and microbes has played an
important role in its successful invasion (Bonthond et al., 2020, 2021;
Saha et al., 2016; S. Wang, Wang, et al., 2017; S. Wang, Weinberger, et
al., 2017). Within native and non-native habitats, G.
vermiculophylla covers wide latitudinal ranges, which are highly
variable in temperature (Sotka et al., 2018). Not surprisingly, it is
tolerant to a relatively wide temperature range. Gracilaria
vermiculophylla has been found to have a thermal growth optimum ranging
from 15 to 25 °C (Nejrup, Staehr, & Thomsen, 2013; Yokoya, Kakita,
Obika, & Kitamura, 1999). At lower temperatures (8 °C), the alga grows
slowly, but can survive for months in dark and nutrient-free conditions,
which may explain its ability to survive long distance transportation
(Nyberg & Wallentinus, 2009). However, qualitative observations
(Weinberger et al., unpublished data) also suggested that the risk of
developing disease symptoms increases at 20 °C and higher.
We collected algal thalli from native and non-native G.
vermiculophylla populations and cultivated these in a common garden at
an optimal growth temperature of 15 °C and an elevated temperature of 22
°C. We specifically tested the hypotheses that (i) G.
vermiculophylla holobionts perform better at 15 °C compared to 22 °C
(i.e., less disease symptoms and more growth) and (ii) epibiota
have lower beta diversity within-populations at 15 °C compared to 22 °C
. In addition, we expected that (iii) non-native algae perform
better at 22 °C and (iv) their epibiota have lower
within-population beta diversity this elevated temperature.