Discussion
Our results show various levels of population structuring across a range
of spatial and temporal scales. Genetic structuring of lake- and
ocean-developing G. brevipinnis populations indicates that lake
populations are generally closed and therefore isolated from downstream
coastal populations over long timescales. Collectively, lake tributary
populations exhibit greater genetic structuring than coastal
populations, but comparatively little genetic structuring is evident
within individual lakes or along the coast, consistent with more open
populations dynamics and within-system exchange of individuals. On
shorter timescales, within-system otolith trace element signatures align
with genetic results, suggesting that no migration occurs between lake
tributary populations and coastal stream populations. Otolith trace
element signatures also indicate further structuring on shorter
timescales, with a semi-closed meta-population structuring of individual
catchments or regions within lake and coastal systems. Larval plume
residence is likely a simple consequence of rheotaxis (Hicks, 2012), a
behavioural mechanism that may generate population isolation and
structuring across both short and long timescales. Due to its ‘leaky’
nature, plume residence may result in populations being closed across
short timescales and driven by self-recruitment, but not sufficient to
prevent limited dispersal and genetic exchange among rivers, leading to
open population dynamics on a longer timescale.
Long-term population
structure
When compared to coastal stream populations in close proximity, lake
tributaries have higher levels of structuring, indicating that each lake
creates a closed population subject to genetic drift. In contrast,
genetic structuring is relatively homogeneous within each lake and
coastal region, indicating that the within-system meta-populations
evident via otolith microchemistry results are not as isolated, and
therefore relatively open, over longer timescales. Patterns of closed
populations in lakes persist even where lakes are in close proximity to,
and have open access to, the marine environment. Thus, lakes appear to
act as barriers to upstream migration, despite presenting no obvious
physical barrier to movement (see Gouskov & Vorburger, 2016).
Mechanisms potentially leading to this isolation are unclear, but could
be related to simple behaviours such as preference for current and
upstream orientation (Hicks, 2012). By preferring to orient into the
current, lake-developing larvae would seem likely to be retained in
their natal river plume, as suggested by our larval trawling results,
and adults and juveniles from downstream diadromous populations are
unlikely to move upstream through a lake due to the absence of
directional cues provided by water currents (Concepcion & Nelson,
1999), thus preventing exchange. Within lake and within-coast
comparisons suggest relatively low genetic structuring, implying that
catchment level meta-populations are open over long timescales, aligning
with other studies on dispersive larvae which find connectivity at broad
spatial and temporal scales (McDowall, 2003; McDowall, 2007).
Short-term population
structure
Otolith trace-element signatures show both distinct system level
population structuring, aligning with genetic results, and within system
meta-population structuring, thus detecting a level of fine-scale
relatively closed populations not detected by genetic methods. Distinct
otolith trace element signatures formed between lake tributaries and
coastal streams are not unexpected in our case due to impermeable
hydro-electric dams downstream of lakes Wanaka and Wakatipu, as well as
the distances involved. Further, a lack of mixing has previously been
found in Lakes Moeraki and Paringa, which both have unimpeded access to
the coast (Hicks et al., 2017), suggesting that connectivity is even
more unlikely when a physical barrier is present. However, distinct
trace element signatures between Lakes Wanaka and Wakatipu suggests
retention within each lake, and therefore a closed population, despite
the absence of any impermeable physical barriers that would prevent
movement between the two. These closed populations must persist long
term, as the same pattern can be seen in the genetic results. In
contrast, both marine and freshwater populations seen in our study also
formed otolith trace element clusters when grouped by tributary or
region, indicating fine scale, catchment-level, semi-closed population
structuring within coast or lake, similar to other studies (Hogan et
al., 2014; Smith & Kwak, 2014; Warburton et al., 2018). Even the less
distinct clusters (e.g. in L. Wakatipu) still had much higher
reclassification success than would be expected if recruitment was
largely from unstructured pools (e.g. Hickford & Schiel, 2016),
suggesting at least some degree of larval philopatry (Warburton et al.,
2018). While genetic population structuring could occur through
mechanisms such as reproductive isolation via altered spawning time, we
observed catchment and lake level structuring in the otolith trace
element signatures of a single cohort. These results suggest behavioural
mechanisms are restricting widespread larval dispersal from their natal
streams, which would also result in retention within lakes.
Larval behaviour as a
mechanism for population structuring
Larval plume residence found in this study suggests a behavioural
mechanism that isolates populations within different streams or regions,
and leads to long term isolation of lake populations. Nearly all larvae
found in the study were present in river plumes, suggesting substantial
retention within each stream draining into a lake or the sea. This
process should result in the formation of semi-closed meta-population
within lakes and along coastlines, concordant with the patterns seen in
otolith trace element signatures. Further, plume residence seemingly
provides a mechanism by which larvae avoid drifting out of lakes (David
et al., 2019; Hicks, 2012), isolating populations within lakes, even
when close to the coast. The actual behaviour maintaining larvae within
plumes is unclear, although the observation of strong rheotaxis even in
newly hatched larvae (Hicks, 2012), could provide a simple explanation
for the retention of larvae in river plumes. Similarly, the river plumes
entering lakes studied here anecdotally appeared to have more
zooplankton than other sites, suggesting food availability may also
favour retention in these systems. River plumes represent dynamic
environments and thus the degree of retention is likely to vary both
spatially between river plumes, and temporally in response to changes in
flow. Similarly rare dispersal events mediated by environmental
conditions have been identified in other systems such as arid
floodplains (e.g. Mossop et al., 2015), resulting in relatively low
genetic structuring despite largely disconnected ecological populations.
Whilst the majority of larvae collected were in river plumes, the
collection of small numbers of larvae in offshore habitats suggests
leakage from river plumes, likely providing a degree of population
connectivity within lake and marine pelagic habitats, thus maintaining
population and hence genetic connectivity resulting in open population
signatures over longer timescales.
Evolutionary
implications
Behaviours that retain larvae within river plumes and resist dispersal
provide a simple mechanism that could interact with landscape to produce
context dependent patterns of population connectivity and isolation.
Collectively, our results form a case study describing how behaviour
might interact with geologic events (Craw et al., 2016) and landscape to
facilitate divergence of landlocked populations of an ancestral G.
brevipinnis, that may have led to the subsequent radiation of the
non-migratory G. vulgaris species-complex (Allibone & Wallis,
1993; Allibone et al., 1996; Burridge, McDowall, Craw, Wilson, &
Waters, 2012; Waters et al., 2010). Our results confirm that
lake-developing populations of G. brevipinnis are isolated and
genetically divergent, despite the relative proximity and potential
connectivity with other lake populations and even diadromous populations
in some cases. Similar speciation patterns are repeatedly seen in other
amphidromous fish which universally have a pelagic larval phase but
isolated adult populations (Augspurger, et al., 2017), including members
of the Cottidae (Dennenmoser, Rogers, & Vamosi, 2014; Goto et al.,
2015), Eleotridae (Nordlie, 2012) and Gobiidae (Keith & Lord, 2011),
which are likely influenced by similar interactions between landscape,
geology and behaviour.
Our results also have implications for the management and conservation
of amphidromous species, particularly those in which non-diadromous
populations are readily formed. Our otolith microchemical results,
indicating that short-term population-sustaining processes may occur at
the scale of individual catchments or isolated geographical regions, add
further weight to the notion that management may have to be undertaken
at the local (Hicks et al. 2017; Warburton et al., 2018) rather than
island or distribution wide (Cook, Bernays, Pringle, & Hughes, 2009)
scale. Further, the translocation of individuals from landlocked
populations of facultatively amphidromous species has been suggested as
a potential management strategy to enhance typically more degraded,
lowland diadromous populations (e.g. David, 2003). Our finding of high
genetic differentiation in landlocked populations, together with
previously identified ecological differences between landlocked and
diadromous populations (Augspurger & Closs, 2019), suggest that such a
strategy should be approached with caution. Indeed, the translocation of
a facultatively amphidromous shrimp before high levels of cryptic
diversity were recognized has been recognized as resulting in the rapid
extinction of the local genotype (Cook et al. 2006; Hughes et al. 2003).