Phylogeography and population genetics
Historically, glacial cycles probably had a strong influence on species
distributions. Most of Iceland‘s shelf was covered by an ice sheet
during the Last Glacial Maximum (~25 ka), which broke up
around 15 ka due to a northward shift of the polar front and rising sea
levels (reviewed by Geirsdóttir et al., 2009). At that time, today’s
pattern of currents was established. The near-shelf populations ofH. bicuspis (represented by stations 1019, 1194 and 1219) were
likely colonized following the break-up of the Icelandic ice shield.
Deep-sea populations farther off the coast may have also been affected
by changing temperatures, currents, etc. The observed demographic
history for H. bicuspis I-III suggests a relatively recent
decline in population sizes followed by a rapid recovery, though we do
not have any age estimates (Figure 5). This overall pattern might
reflect population declines and local extinctions during the Last
Glacial Maximum. This was then followed by population expansions and
recolonizations from unaffected deep-sea regions farther off the coast
during the Holocene, which were scarcely sampled in our study.
Colonization from less affected regions might also explain the rapid
recovery of population sizes.
Our data suggests a complex colonization history of the near-shelf
regions north of the GIF Ridge for all three lineages observed withinH. bicuspis I-III. The consistently observed differences between
the mitochondrial COI and nuclear ddRAD data imply differing migration
behavior between males and females. The maternally inherited COI
exhibited consistently higher levels of genetic differentiation between
populations, which suggests males migrate more actively and potentially
over wider distances, while females appear to be rather stationary. This
is surprising, as Haploniscus bicuspis does not exhibit a strong
sexual dimorphism in swimming structures as observed in other isopod
families (e.g., Brix et al., 2020; Bober et al., 2018; Hessler, 1970;
Riehl, Wilson, & Hessler, 2012). However, adult males of H.
bicuspis have stouter second antennae with many more sensory sensilla
and aesthetascs than females or juvenile and preparatory males. This
difference was not described by Brökeland & Wägele (2004), as they did
not have adult males available in the type series. The aesthetascs are
hypothesized to have a chemosensory function, possibly enabling males to
detect females across large distances. This suggests that males have a
more active lifestyle, roaming around in search for females, which would
explain the inferred sex-specific migration patterns and the different
distribution patterns of COI and ddRAD lineages. As stated in Brix et
al. (2020), locomotion of the adult stages does influence migration
patterns and distance for Pacific isopod families, but also a “male
behavior” is reflected in the Pacific data for Haploniscidae.
The ‘central’ region north of the GIF Ridge around stations 1194 and
1219 was probably first colonized by lineage II, possibly originating
from close-by populations in the Norwegian Sea to the east or north-east
of Iceland. Subsequently, males from northern (lineage III) and southern
(lineage I) populations migrated into the area around station 1219,
largely replacing the local population. The result is a local population
at station 1219 that comprises a hybrid nuclear genome of lineages I and
III, but the mitochondrial genome of lineage II. These newly arriving
males must have outnumbered the local (male) population or were better
adapted to the local environmental conditions, or both. We propose a
similar scenario for the north-eastern populations around stations 1159
and 1172. These were probably first colonized by lineage I, possibly
from the central or southern Norwegian Sea, with subsequent male-biased
migration and introgression from lineage II, resulting in populations
with lineage I mitochondrial and lineage II nuclear genomes. The
reverse, a female-biased migration and introgression, is highly unlikely
in both cases due to the overall higher rates of population
differentiation in COI (suggesting lower female migration rates) and
because in such a scenario these females should have contributed to the
nuclear genome as well.
Overall, our results show that genetic differentiation between
populations is usually high, even at comparably low geographic
distances, suggesting low dispersal and gene flow rates. This is also
supported by elevated inbreeding coefficients in some populations,
implying that reproduction occurs frequently among closely related
individuals. The above-described hybridization scenarios appear to
represent rare events, which probably occurred at a time when local
population densities were still low in the early phase of
recolonization. The strongly male-biased migration behavior is
noteworthy, with the only apparent sexual dimorphism in sensory
structures. If such patterns hold true for other asellote isopods,
population differentiation inferred from mitochondrial markers like COI
might systematically underestimate dispersal and gene flow rates.
Haploniscus bicuspis IV is the only putative species with
consistently positive values in Tajima’s D and Fu’s Fs, suggesting that
it is currently undergoing a genetic bottleneck. At least in COI, this
putative species appears closer related H. bicuspis I-III, which
occurs exclusively in colder arctic waters. It is possible that H.
bicuspis IV is also better adapted to colder temperatures and is
negatively affected by the northward movement of the Arctic front
throughout the Holocene. The ranges of H. bicuspis IV and V meet
along the Reykjanes Ridge, and we found H. bicuspis V at most
stations, but with less genetic diversity among those found at the
Reykjanes Ridge stations. Whether both species coexist due to the
topological, structural, and environmental diversity of the Reykjanes
Ridge (German et al., 1994; Taylor et al., in review) or whetherH. bicuspis V is currently replacing H. bicuspis IV is an
unanswered and interesting question.