i. Title:
Migration-tracking integrated
phylogeography supports long-distance dispersal-driven divergence for a
migratory bird species in the Japanese archipelago
ii. A short running title:
Divergence scenario for a Japanese migrant
iii. Author:
AOKI Daisuke1, SAKAMOTO Haruna1,
KITAZAWA Munehiro2, KRYUKOV Alexey
P3 & TAKAGI Masaoki4,*
iv. Author’s institutional affiliations
1Department of Natural History Sciences, Graduate
School of Science, Hokkaido University, N10W8, Kita-ku, Sapporo
060-0810, Japan
2Frontiers in Environmental Sciences, Graduate School
of Agriculture, Hokkaido University, N9W9, Kita-ku, Sapporo 060-8589,
Japan
3Laboratory of Evolutionary Zoology and Genetics,
Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far
Eastern Branch of the Russian Academy of Sciences, Vladivostok 690022,
Russia
4Department of Natural History Sciences, Faculty of
Science, Hokkaido University, N10W8, Kita-ku, Sapporo 060-0810, Japan
* Correspondence: email address mtakagi@eis.hokudai.ac.jp, telephone
number +81(11)706-4464
ORCID: AOKI Daisuke, 0000-0002-5780-8487
TAKAGI Masaoki, 0000-0001-8308-899X
KRYUKOV Alexey P, 0000-0001-7010-7338
v. Acknowledgements
We thank Hiroaki Matsumiya, Seiichi Hara, Sachiko Endo, Junco Nagata,
Yaroslav A. Red’kin, Ivan M. Tiunov, and Yamashina Institute for
Ornithology for providing us with samples of shrikes from various
regions. The manuscript was greatly improved by valuable comments from
Professor Itsuro Koizumi, Keisuke Atsumi, and laboratory members of the
Biodiversity course, Hokkaido University. Analyses were greatly improved
using high throughput computers, which Professor Itsuro Koizumi,
Professor Hiroshi Kajihara, Professor Toru Kato and Professor Keiichi
Kakui kindly allowed us to use. We are grateful for the considerable
help received from many daily field assistants: Noritomo Kawaji,
Takayuki Kawahara, Yusuke Nishida, Mari Esashi, Ryotaro Sato and Riku
Chiba. This study was partly conducted with a support of a grant-in-aid
for Scientific Research (C) to MT (no. 16K14796 and 16H04737) and to DA
(no. 19J21406) from the Japanese Society for the Promotion of Science
(JSPS).
vi. Abstract and keywords:
Aim : In theory,
long-distance dispersal (LDD) outside a species’ range contributes to
genetic divergence. However, previous studies have not discriminated
this process from vicariant speciation in migratory bird species. We
conducted an integrative phylogeographic approach to test the LDD
hypothesis, which predicts that a Japanese migratory bird subspecies
diverged from a population in the coastal region of the East China Sea
(CRECS) via LDD over the East China Sea (ECS).
Location : East Asia
Taxon : Brown Shrike (Lanius cristatus )
Methods : Both a haplotype network and a multi-locus gene
network of its three subspecies were reconstructed to examine from which
continental population the Japanese subspecies diverged. A species
distribution model (SDM) for the Japanese subspecies was constructed
using bioclimatic variables under the maximum entropy algorithm. It was
projected to the climate of the last glacial maximum (LGM) to infer the
candidate source area of colonisation. A migratory route of the Japanese
subspecies, which possibly reflects a candidate past colonisation route,
was tracked by light-level geolocators.
Results : Molecular phylogenetic networks suggest that the
Japanese subspecies diverged from a population in the CRECS. The SDM
inferred that the emerged continental shelf of the ECS and the present
CRECS were suitable breeding areas for the Japanese subspecies during
the LGM. A major migratory route for the Japanese subspecies was
inferred between the CRECS and the Japanese archipelago across the ECS.
Main conclusions : Our integrative approach supported the LDD
hypothesis for divergence of the Japanese subspecies of the Brown
Shrike. Shrinkage and expansion of the ECS may have been responsible for
successful colonisation and isolation of the new population. Vicariance
was inferred for divergence of the subspecies in the northeast Asian
continent from the Japanese population. Our framework provides a new
phylogeographic scenario in this region, and discriminating LDD and
vicariance models should improve our understanding of the
phylogeographic histories of migratory species.
Keywords: Light-level geolocator, long-distance dispersal,
migratory route, phylogeography, species distribution modelling, the
Brown Shrike, the Japanese archipelago, vicariance
vii. Main text
Introduction:
High dispersal propensities due to animal migratory behaviour, and how
they contribute to speciation, is an infrequently studied area of
biogeography (Greenberg & Marra, 2005; Winger, Auteri, Pegan, & Weeks,
2019). High dispersal ability often leads to long-distance dispersal
(LDD) well outside a species’ known range. This phenomenon is called
vagrancy and derives mostly from migratory populations that have, for
instance in the case of birds, drifted past or overshot their
anticipated destinations, influenced by wind during their seasonal
migration (Newton, 2008). In theory, the frequency of vagrancy is a key
determinant of its effect on a population that receives vagrants (Rose
& Polis, 2000). A high frequency of vagrancy may increase the chance of
successful establishment of an allopatric population (O’Connor, 1986;
but see Lees & Gilroy, 2014), whereas it may prevent isolation of the
new population and hence preclude genetic divergence (Harvey et al.
2019). Paleogeographical change is a candidate mechanism that allows
divergence of a new population since it changes the frequency of LDD
over geological timescales (Weeks & Claramunt, 2014). For example,
vagrancy will decrease in frequency when a geographic barrier between
the source and new populations expands, because vagrancy decreases with
increasing distance (Lees & Gilroy, 2014; O’Connor, 1986). Many
phylogeographic studies of migratory species, however, have anecdotally
assumed that previously known biogeographical barriers subdivided a
formerly continuous population, i.e. vicariance (e.g. Weir & Schluter,
2004; Zink, Pavlova, Rohwer, & Drovetski, 2006). While vicariance has
provided sufficient explanations for many cases of genetic divergence of
migratory species, an alternative scenario — that a paleogeographical
change facilitated LDD-driven divergence — has never be empirically
tested. This might be because many currently migratory bird species are
continental and widespread (Somveille, Rodrigues, & Manica, 2018), thus
their phylogeographic processes of speciation could have hardly be
inferred without the assumption of vicariance (Albert, Schoolmaster,
Tagliacollo, & Duke-Sylvester, 2017).
Owing to its insular nature, well-documented paleogeography, and
relatively high endemism of breeding migratory passerine lineages
(Saitoh et al., 2010, 2015), the Japanese archipelago provides a
suitable system within which to identify a biogeographic mode of
speciation of a migratory lineage. During glacial periods of the
Quaternary (approximately 2.7 million years ago to the present), due to
lower sea levels, some parts of the Japanese archipelago were connected
to the continent via land bridges, while other parts remained separated
(Gallagher et al., 2015; Matsuzaki, Itaki, & Tada, 2019; Ohshima, 1990;
Ota, 1998). Most terrestrial animal species currently occurring in Japan
colonized the archipelago from the East Asian continent during glacial
periods, and they subsequently diverged as Japanese endemics (McKay,
2012; Motokawa, 2017). Moreover, source continental populations could be
either on the coastal region of the East China Sea (CRECS) or northeast
Asian continent (the Korean Peninsula, northern China to Far East
Russia), where different species or populations occupy their breeding
ranges (e.g. Dong et al., 2015; Päckert et al., 2011; Saitoh et al.,
2015; Zhao et al., 2017). This system, predicting from which regional
population and along which route the Japanese archipelago was colonized,
will help indicate which of the two following hypotheses is more
plausible. 1) Colonisation across the open East China Sea (ECS) from the
CRECS, implying LDD-driven divergence; hereafter called the LDD
Hypothesis (Figure 1a). 2) Colonisation by means of a range shift over a
land bridge from the Korean Peninsula to Japan (where there is currently
the Tsushima Strait), implies that the disappearance of the land bridge
led to vicariant speciation; hereafter called the Vicariance Hypothesis
(Figure 1b).
We conducted integrative phylogeography by means of phylogenetic
networks, a species distribution model (SDM), and migration tracking
using light-level geolocators, to infer the past colonisation of the
Japanese archipelago. Phylogenetic networks are informative for
disentangling relationships of intraspecific genetic variations both in
haplotype and multi-locus data (Huson & Bryant, 2006; Mardulyn, 2012).
SDMs can infer suitable breeding distributions of species during the
last glacial maximum (LGM), ca. 20,000 years ago (20 kya) from present
species distributions (Elith et al., 2011). Any continental range that
was also suitable during a glacial period may be interpreted as a
potential area from which colonisation occurred (Zink & Gardner, 2017).
An avian migratory route over a sea barrier between the Japanese
archipelago and the Asian continent may be interpreted as a candidate
for the past colonisation route to the Japanese archipelago for the
following reasons. First, an existing migration route over a large
geographic barrier may reflect LDD in the past when the barrier was
smaller or absent (Newton, 2008; Winger et al., 2019). Second, the
migratory route also partly retraces past shifts in the breeding range
(Alvarado, Fuller, & Smith, 2014; Newton, 2008; Ruegg, Hijmans, &
Moritz, 2006; Winger et al., 2019). Therefore, both modes of past
colonisation may be reflected in the migratory route over a present sea
barrier in this system.
Results of the three components can be differently predicted from the
LDD and vicariance hypotheses in this framework. (1) The LDD hypothesis
predicts that a genetic split between the archipelagic population and a
population in the CRECS will be inferred by phylogenetic networks. For
the archipelagic population, CRECS is predicted to have been suitable
during the glacial period by the SDM, and a migratory route across the
ECS between the Japanese archipelago and the CRECS is expected to have
been likely (Figure 1a). (2) The vicariance hypothesis predicts that the
archipelagic population genetically nests within, or is not well
divergent from, the population in the northeast Asian continent, because
the land bridge between the Korean Peninsula and the Japanese
archipelago repeatedly formed and disappeared. For the archipelagic
population, either current northern China or the Korean Peninsula are
predicted to have been suitable during a glacial period by the SDM, and
a migratory route is expected over the Korean Peninsula from and to the
Japanese archipelago (Figure 1b).
We studied a long-distance migratory passerine, the Brown Shrike
(Lanius cristatus ), as our first attempt to test these hypotheses
given the breeding distribution of its three subspecies. L. c.
superciliosu s breeds in the Japanese archipelago, L. c.
lucionensis breeds in the CRECS, and L. c. cristatus breeds in
the northeast Asian continent and most of Sakhalin Island (Figure 1c;
Lefranc & Worfolk, 1997). With a dated phylogenetic tree, we provided a
phylogeographic scenario of the divergence of the Brown Shrike based on
the results obtained from our integrative approach. From this scenario,
we discuss the paleogeographical context in which LDD could have
contributed to the genetic divergence of a migratory species.
Materials and Methods:
Study species and field
procedure
To track the migratory routes of L. c. superciliosus , we captured
25 adult male shrikes in Hokkaido and marked them with leg rings. We
attached MK5740 geolocator tags (BioTrack) with leg-loop harness strings
(Rappole & Tipton, 1991). We ensured that the total mass of the system
(< 1.1 g) did not exceed 5% of the birds’ mass (Bridge et
al., 2013). Eight birds (32%) returned to the breeding study site in
2018. Deployment of tags did not significantly change the return rate
when compared with a previous report by Takagi (2003) (chi-square test
for independence; χ2 = 0.11, df = 1, p = 0.74). Four
males lost their tags before recapture. One male marked with leg rings
disappeared before breeding in 2018 and did not return to the site in
2019, so it remained uncaptured (the presence of this bird’s geolocator
was not confirmed).