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).