Introduction
Processes responsible for population structuring are key to
understanding population dynamics and speciation. Isolation occurs on a
continuum from longer, multi-generational timescales, whereby
populations genetically diverge through selection and genetic drift, to
much shorter timescales (even a single generation), when immigration is
rare enough to produce distinct ecologically closed (i.e.
self-recruiting) populations, that may still maintain genetic
connectivity over the long term (Dunning, Danielson, & Pulliam, 1992;
Kekkonen et al., 2011; Slobodkin, 1980; Jones et al., 2009).
Furthermore, genetic shifts may occur through strong selection acting
over relatively short timescales (Carroll, Hendry, Reznick, & Fox,
2007; Fussmann, Loreau, & Abrams, 2007), despite populations
maintaining some genetic connectivity (Moody et al., 2015). As a result,
it is often difficult to determine the degree and timescale at which
population connectivity occurs (Fussmann et al., 2007; Levin, 1992).
Therefore, evaluating both short- and longer-term population structuring
is key in determining both ecological and evolutionary dynamics. To
determine why population structuring occurs and differs on various
spatial and temporal scales, the mechanisms driving population
structuring must also be examined (Levin, 1992).
Behaviour and life history traits can interact with landscape and
generate context-dependent patterns of isolation, and therefore
population structure, across various temporal scales. Dispersive or
migratory behaviours (Cowen, Lwiza, Sponaugle, Paris, & Olson, 2000;
Dingle & Drake, 2007) tend to maintain open populations, where
individuals are often exchanged. (Pinsky et al., 2017). If migratory
pathways fragment and behavioural mechanisms favour local retention as
opposed to connectivity, isolation may occur causing open populations to
become closed (self-recruiting) (Booth, Montgomery, & Prodöhl, 2009;
Hughes, Schmidt, Macdonald, Huey, & Crook, 2014). Understanding
behavioural mechanisms is essential in instances where structured
populations form despite no apparent barriers to genetic exchange or
structuring mechanisms (Levin, 1992).
Amphidromous fishes provide an ideal system to investigate behavioural
mechanisms leading to open and closed population structuring across
timescales due to the combination of stream resident adults and a
potentially dispersive marine pelagic larval phase (Augspurger,
Warburton, & Closs, 2017; McDowall, 2007). Amphidromous fishes spawn in
freshwater. After hatching, larvae drift downstream to a marine pelagic
environment, develop for a period of typically 3–6 months, then return
to freshwater fluvial environments as juveniles where they remain for
life. Many such species are thought to disperse during the larval phase
and maintain open populations across broad geographic distributions
(McDowall, 2003, 2007). In contrast, other species appear to resist
dispersal, resulting in relatively closed populations across short
(Hogan, Blum, Gilliam, Bickford, & McIntyre, 2014; Sorensen & Hobson,
2005; Warburton, Jarvis, & Closs, 2018) and even long timescales
(Hughes et al., 2014) despite no obvious barriers preventing
connectivity.
Amphidromous fishes also often form landlocked populations, the
life-history of which is nearly identical to their diadromous
counterparts, with fluvial juvenile and adult forms and pelagic larvae.
In this case, however, larval development occurs in a lake rather than
the marine environment (Augspurger et al., 2017). This landlocking
provides further potential for closed and open population structuring
across timescales, as lakes can provide an opportunity for the isolation
and genetic divergence of populations (Gouskov & Vorburger, 2016; King,
Young, Waters, & Wallis, 2003). Closed landlocked populations diverge
further genetically, subsequently radiating into non-migratory forms and
species complexes (Allibone & Wallis, 1993; Allibone et al., 1996;
Burridge, McDowall, Craw, Wilson, & Waters, 2012; Goto, Yokoyama, &
Sideleva, 2015; Yamasaki, Nishida, Suzuki, Mukai, & Watanabe, 2015). In
other cases, landlocked populations maintain connectivity with
diadromous populations across longer-term timescales (Goto & Arai,
2003; Hicks et al., 2017). Behavioural mechanisms during the larval
pelagic phase, such as orienting into current, may play a role in
determining connectivity across both short- and long timescales.
Galaxias brevipinnis is a facultatively amphidromous fish
distributed throughout New Zealand, with great capacity for forming both
diadromous and landlocked populations (McDowall, 1990). Landlocked
populations of G. brevipinnis are potentially isolated from
diadromous populations as their larvae develop in lakes, but do not
appear to drift downstream out of them (Hicks et al., 2017). This may be
due to their strong rheotactic behaviour after hatching, which may limit
dispersal from their pelagic developing environment (Hicks, 2012).
Further, diadromous adults are rarely found upstream of lakes, despite
the absence of any obvious in-stream barriers blocking access, possibly
due to the lack of a rheotactic cue allowing juveniles to navigate
through large pelagic environments (Hicks, 2012; Jarvis & Closs, 2019).
Thus, populations of G. brevipinnis may potentially exhibit
context-dependent degrees of population isolation and genetic
structuring, creating an ideal opportunity to examine the importance and
interaction of behaviour and landscape on population connectivity across
temporal and spatial scales.
Here we investigate patterns of hierarchical population structuring inG. brevipinnis across spatial and temporal scales, and the
possible role of behaviour in generating population structuring. We use
genetic analyses to determine population structure across long
multi-generational timescales, analysis of otolith trace element
signatures to evaluate population structure over short timescales (the
processes sustaining a population over a single generation), and larval
trawling to determine larval distribution as a result of behaviour. We
hypothesized that population structuring would interact with landscape,
and generated a number of hypotheses in this context. Over long
timescales, we predicted that: (1) coastal populations would tend to
show high genetic homogeneity, indicating open populations like those of
other amphidromous fishes, while (2) landlocked populations would show
closed populations and some genetic divergence from other landlocked
populations and coastal sites. Over short timescales, we hypothesized
that: (3) landlocked and coastal stream populations would develop within
their respective systems (e.g. lake or ocean), and (4) otolith trace
element signatures would reflect catchment level meta-populations within
lakes and along coastlines, forming semi-closed (self-recruiting)
populations on short-term timescales that are isolated to varying
degrees despite some level of genetic exchange across longer-timescales.
Finally, we hypothesized that: if otolith clustering occurred, (5)
larval distribution would show higher larval densities in river plumes.