Possible LDD-driven divergence process of migratory species
Previous studies have illustrated a divergence scenario for migratory
species that assumed vicariance in generating isolated populations
(Hewitt, 2004; Weir & Schluter, 2004). While this scenario has provided
suitable explanations for many cases, some divergence events may not
adequately be explained by it. For example, the traditional vicariance
scenario suggests that the 100 km wide strait between the Korean
Peninsula and the Japanese archipelago caused deep genetic divergence of
archipelagic populations of mammals from the continent (McKay, 2012;
Sato, 2017). From an ecological perspective, such a small barrier would
ineffectively restrict the movement of a highly volant bird species
(e.g. Gotelli & Graves, 1990), and establishment of a new population
from a more distant area as a consequence of LDD is likely to be its
alternative explanation. However, traditional frameworks based on the
continental distribution for most migratory species have probably
hindered the opportunities to test it (Warren et al., 2015).
Our integrative approach using a Japanese migratory bird species
provided a suitable system within which to discriminate the mode of
genetic divergence under a hypothesis testing framework. We successfully
provided a hypothetical scenario for how LDD and paleogeography have
contributed to divergence of a migratory species. We also showed that
discriminating LDD from vicariance in our framework benefited a more
comprehensive understanding of diversification mechanisms of migratory
species in this region. We believe that consideration of LDD is also
important for continental regions where most migratory species have
diversified. Attention has recently been paid to LDD and colonisation as
an important phenomenon for distribution and speciation of continental
migratory species (Rushing, Dudash, Studds, & Marra, 2015; Winkler et
al., 2017). Like the ECS in our system, some geographic barriers (such
as seas, deserts, and mountain ranges) in continental areas have also
changed size and shape during their geological history (Hewitt, 2004;
Sun et al., 2018). Some of the genetic divergence in migratory species
over these barriers should be revisited taking the LDD hypothesis into
account (e.g. Reeves, Drovetski, & Fadeev, 2008). Further verification
of the usability of our integrative approach among several species will
facilitate our understanding of the relative importance of LDD to
vicariance in the speciation of migratory birds and other animals.
ix. Figures embedded in the text:
Figure 1 Predicted colonisation route (black arrows) and
expected results from integrative approaches in (a) long distance
dispersal (LDD) and (b) vicariance hypotheses in the Brown Shrike.
Predicted gene networks (upper left panes), migratory routes (lines with
open circles), and suitable glacial regions (coloured circles) under the
two hypotheses are shown. Colours correspond to subspecies in Figure 1c.
We predicted that L. c. lucionensis represents the basal lineage
of the Brown Shrike since close relatives of this species are
distributed around South-east Asia (Zhang et al., 2007). Because there
are various possibilities for the genetic position of L. c.
cristatus in the LDD hypothesis, we did not present it in Figure 1a.
Grey coloured regions represent terrestrial areas during the Early to
the Middle Pleistocene, and dotted lines indicate the present
coastlines. (c) DNA sampling localities. Circles and triangles represent
samples from breeding and non-breeding localities, respectively, and
their colours indicate haplogroups inferred in the median-joining
haplotype network of COI (Figure 2a). Land colours indicate breeding
ranges of presumed subspecies following Worfolk (2000). The striped
region indicates a presumed hybrid zone between subspecies.
Figure 2 (a) A median joining haplotype network constructed
using 521 bp of the partial COI gene. Each circle indicates a unique
haplotype and its size is proportional to the number of samples. Colours
of circles indicate regions where samples were collected. One mutational
gap was indicated by one bar, and a black node indicates a median
vector. Clusters analogous to clades found in the Bayesian inference
tree (Figure S1.2) are indicated. (b) The multi-locus network
constructed for the Brown Shrike using the four loci under the
NeighborNet algorithm. Coloured shades correspond to clades to which
their mitochondrial haplotypes belong.
Figure 3 Estimated suitable distribution for L. c.superciliosus for different time periods; a constructed model was
projected to (a) the present climate, and (b-d) three different climate
models for the Last Glacial Maximum (LGM, 20 kya). Suitability for a 2.5
min grid increases from yellow, green to indigo, whereas the grey area
was determined as absence. The black area is that of strict
extrapolation indicated by multivariate environmental similarity surface
analysis. Black lines indicate present coastlines. Note that the
terrestrial landmass expanded during the LGM due to the lowered sea
level.
Figure 4 Migratory routes of three individual L. c.
superciliosus around the East China Sea. Mean posterior probabilities
of location estimates of the three birds for each raster cell are
indicated by colour gradation from yellow (high) to indigo (low). Dots
with line segments indicate median tracks of their inferred migratory
routes (white and red dots indicate migrating and stationary sites,
respectively). Autumn and spring migrations are indicated by solid and
hatched lines, respectively.
Figure 5 Schematic presentation of the hypothetical
phylogeographic scenario of divergence in the Brown Shrike. (a) The
ancestral population colonised the Japanese archipelago via LDD across
the East China Sea (ECS) in a glacial period around the late Early
Pleistocene. (b) Increased isolation of the archipelagic population
through expansion of the ECS facilitated its divergence. Its migratory
route was shaped to retrace the colonisation route. (c) In a later
glacial period, part of the archipelagic population colonised the Korean
Peninsula over a land bridge. (d) Northward expansions caused vicariance
of both the archipelagic and northern clades and resulted in their
present geographical distributions. The hatched lines in each pane
indicate the predicted coastlines in the previous inter/glacial periods,
following Ota (1998). Coloured circles indicate ancestral populations of
each lineage. Lines with open circles indicate the migration route and
arrows indicate movements of populations.