Introduction
Amphibians have suffered immense rates of population declines and
extinctions over recent decades (Houlahan et al. 2000; McCallum
2007; Grant et al. 2019) and are considered the most threatened
vertebrate class on the planet (Howard & Bickford 2014). A significant
contributor to that mortality has been the invasive chytrid fungus
(Batrachochytrium dendrobatidis ), which attacks the host’s
epidermis (Lötters et al. 2009; Fisher & Garner 2020). The
catastrophic impact of chytrid has drawn attention to the vulnerability
of anurans to a diverse array of pathogens, such as ranaviruses (Grayet al. 2009) and parasites (Hartson et al. 2011; Gustafsonet al. 2018). In response to challenges induced by pathogens,
anurans exhibit several lines of defense including immune responses and
behavioral avoidance of pathogens (Hossack et al. 2013;
Koprivnikar et al. 2014; McMahon et al. 2014). Moreover,
amphibian skin secretions consist of secretions produced by the
amphibian itself (Clarke 1997) and skin microbiota (mostly bacteria
(Federici et al. 2015)), hereafter, we refer to this combination
as ‘skin secretions’. These secretions contain many antimicrobial
properties (Gustavo Tempone et al. 2007; Govender et al.2012), which might help to fight off pathogens (Weitzman et al.2019; Christian et al. 2021). Simultaneously, pathogens are under
selection to overcome those barriers, generating an ‘arms race’ of
adaptations and counter-adaptations in the host and its adversaries
(Sorci & Faivre 2008). Those host-parasite interactions may drive the
rapid evolution of spatial variation in the attributes of both
participants, and selection should favor hosts that can either tolerate
infection (limiting the harm caused by a given parasite infection) or
reduce infection probability and burden, i.e., resistance (Råberget al. 2009).
Although some studies showed that amphibian skin secretions contain
properties to resist chytrid fungus (Rollins-Smith 2009; Niederleet al. 2019) and bacteria (Quintana et al. 2017), little
is known about the role of secretions as parasite defense mechanisms
more generally. Similarly, we know little about how parasitic nematodes
find their hosts. Generally, nematodes can utilize olfaction, gustation,
thermosensation, and humidity to locate hosts, which they seek via
strategies ranging from ambushing to actively crawling toward
host-emitted cues (Castelletto et al. 2014; Gang & Hallem 2016).
If such strategies for infection avoidance (in hosts) and host
detection/recognition (in parasites) exist, they are expected to vary
geographically between different populations, due to co-evolved local
adaptations between host and parasite which occur on small spatial
scales (Schmid-Hempel 2011).
Biological invasions provide unparalleled opportunities to investigate
arms races between hosts and their parasites, because they create
spatial heterogeneity in transmission rates and impose novel selective
forces on one or both participants. Recently, we showed that the
invasion of cane toads (Rhinella marina , Fig. 1) through tropical
Australia has generated substantial spatial divergence in host-parasite
interactions (Kelehear et al. 2012; Brown et al. 2016;
Mayer et al. 2021). The toads have carried with them a
native-range lungworm (Rhabdias pseudosphaerocephala , Fig. 1)
(Dubey & Shine 2008; Selechnik et al. 2017) that can reduce
viability of the host (Kelehear et al. 2011; Finnerty et
al. 2018). The risk of parasite infection has been modified by the
invasion process, with low population densities of hosts at the
invasion-front reducing opportunities for parasite transfer among toads
(Phillips et al. 2010). Apparently as a result, toads at the
western invasion-front have evolved a greater resistance to parasite
infection (Mayer et al. 2021), and nematodes close to the
invasion-front have evolved a higher infectiviy (Kelehear et al.2012), continuing the arms race. That situation provides an ideal
opportunity to investigate the biological role of anuran skin secretions
in host-parasite interactions.
Because both parasites and their hosts adapt to local conditions,
geographic variation in the skin secretions of cane toads might have
both positive and negative consequences for host fitness. Skin
secretions might render it more difficult for a parasite to infect their
host, if secretions inhibit the parasite’s ability to locate and/or
enter the host’s body or find its way to the target organ where it can
grow and mature (here termed the ‘host defense ’ hypothesis).
Alternatively, the parasite might evolve to use the host’s skin
secretions as a signal for host location, or as a cloak to hide from the
host’s immune system during the parasite’s migration through the body of
the host (here termed the ‘parasite cue ’ hypothesis). Notably,
these two hypotheses are not entirely exclusive; for example, skin
secretions might facilitate host location by the parasite, but still
defend against penetration by the parasite. By studying a system where
host-parasite interactions have diverged rapidly, we have an opportunity
to detect a range of such outcomes. We conducted experiments to (1)
clarify the role of toad skin secretions as a host-finding cue for
lungworms, and (2) test the function of toad skin secretion as defense
mechanism against parasite infection (Table 1).