G C A T T A C G G C A T genes Article Waves Out of the Korean Peninsula and Inter- and Intra-Species Replacements in Freshwater Fishes in Japan Shoji Taniguchi 1 , Johanna Bertl 2, Andreas Futschik 3 , Hirohisa Kishino 1 and Toshio Okazaki 1,* 1 Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan; [email protected] (S.T.); [email protected] (H.K.) 2 Department of Mathematics, Aarhus University, Ny Munkegade, 118, bldg. 1530, 8000 Aarhus C, Denmark; [email protected] 3 Department of Applied Statistics, Johannes Kepler University Linz, Altenberger Str. 69, 4040 Linz, Austria; [email protected] * Correspondence: [email protected] Abstract: The Japanese archipelago is located at the periphery of the continent of Asia. Rivers in the Japanese archipelago, separated from the continent of Asia by about 17 Ma, have experienced an intermittent exchange of freshwater fish taxa through a narrow land bridge generated by lowered sea level. As the Korean Peninsula and Japanese archipelago were not covered by an ice sheet during glacial periods, phylogeographical analyses in this region can trace the history of biota that were, for a long time, beyond the last glacial maximum. In this study, we analyzed the phylogeography of four freshwater fish taxa, Hemibarbus longirostris, dark chub Nipponocypris temminckii, Tanakia ssp. and Carassius ssp., whose distributions include both the Korean Peninsula and Western Japan. We found for each taxon that a small component of diverse Korean clades of freshwater fishes Citation: Taniguchi, S.; Bertl, J.; migrated in waves into the Japanese archipelago to form the current phylogeographic structure of Futschik, A.; Kishino, H.; Okazaki, T. biota. The replacements of indigenous populations by succeeding migrants may have also influenced Waves Out of the Korean Peninsula and Inter- and Intra-Species the phylogeography. Replacements in Freshwater Fishes in Japan. Genes 2021, 12, 303. https:// Keywords: competitive exclusion; East Asia; freshwater fish; intra-species replacement; island doi.org/10.3390/genes12020303 model; migration Academic Editors: Tomasz Szwaczkowski and Martino Cassandro 1. Introduction Inter- and intra-species interactions can influence biogeographical distributions [1–3]. Received: 22 December 2020 Among many forms of biotic interactions, replacement among competing species that are Accepted: 18 February 2021 mutually exclusive is presumed to be an important factor in biogeography [4]. Gutiérrez Published: 21 February 2021 et al. (2014) [5] detected the interspecific competition on the biogeography of two mouse opossum species in South America by noting the dominant distribution of one species, Publisher’s Note: MDPI stays neutral whereas another species could potentially distribute. For humans, it has been reported with regard to jurisdictional claims in that series of waves of man originated in Africa and propagated around the world. When published maps and institutional affil- these waves interacted with pre-existing populations, hybridizations and sometimes re- iations. placements occurred along the way in a phenomenon known as “out of Africa” [6,7]. While evidence for segregation is identified as genetic differentiation between geo- graphical regions, phylogeographic evidence of intra-species replacements due to com- petition has not been extensively examined. Most evidence supporting the existence of Copyright: © 2021 by the authors. species replacement is found in the spatial division and isolation of species, where the Licensee MDPI, Basel, Switzerland. distributions of one species are surrounded by those of another [5]. This contrasts with This article is an open access article conventionally observed fragmentation, where populations are both genetically and spa- distributed under the terms and tially isolated from each other. Because fragmented populations are small, they have large conditions of the Creative Commons Attribution (CC BY) license (https:// genetic differentiation. They do not comprise a monophyletic group in phylogeny, but are creativecommons.org/licenses/by/ interspersed by the main population. Conversely, local populations that have been recently 4.0/). Genes 2021, 12, 303. https://doi.org/10.3390/genes12020303 https://www.mdpi.com/journal/genes Genes 2021, 12, x FOR PEER REVIEW 2 of 20 differentiation. They do not comprise a monophyletic group in phylogeny, but are inter- spersed by the main population. Conversely, local populations that have been recently Genes 2021, 12, 303 2 of 18 divided by competitors of a different clade are genetically homogeneous and comprise a monophyletic group (Figure 1). divided by competitors of a different clade are genetically homogeneous and comprise a monophyletic group (Figure1). Figure 1. Schematic illustration of conventional fragmentation and replacement. (a) Conventional fragmentation, where fragmentedFigure 1. Schematic populations illustration diverge into of convention small populationsal fragmentation with unique and genetic replacement. features. (a Isolated) Conventional populations fragmentation, do not comprise where monophyleticfragmented populations groups in the diverge phylogeny into small but are populations interspersed with by unique the main genetic population. features. (b Isolated) Local populations populations (threedo not small com- circlesprise monophyletic and upper and groups lower in fragments the phylogeny colored bu byt are orange) interspersed recently by divided the main by population. competitors (b from) Local different populations clades (three are geneticallysmall circles homogeneous and upper and and lower comprise fragments monophyletic colored by groups. orange) recently divided by competitors from different clades are genetically homogeneous and comprise monophyletic groups. The Japanese archipelago is located at the periphery of the continent of Asia. The archipelagoThe Japanese landmass archipelago originally formedis located the at eastern the periphery margin ofof the the continent continent of of Asia. Asia. After The thearchipelago back-arc landmass of the archipelago originally openedformed the to abouteastern 17 margin Ma, the of the northeastern continent of half Asia. rotated After counter-clockwise,the back-arc of the archipelago while the southwestern opened to ab halfout 17 rotated Ma, the clockwise. northeastern The half current rotated position coun- waster-clockwise, reached at while about 14the Ma southwestern [8] and fused half into rotated the current clockwise. Japanese The archipelagocurrent position at about was 6reached Ma. The at boundary about 14 Ma between [8] and these fused northeastern into the current and Japanese southwestern archipelago masses at is about called 6 theMa. FossaThe boundary Magna (Figure between2a). these The Japanese northeastern archipelago and southwestern is elongated masses in a bow is called along athe north– Fossa southwestMagna (Figure axis. The2a). mountainsThe Japanese extending archipelago along is this elongated archipelago in a bow generate along numerous a north–south- short riverswest thataxis. dischargeThe mountains separately extending into the along ocean. this The archipelago Sea of Japan generate is deep andnumerous has isolated short theriv- islandsers that from discharge the continent separately of Asia, into the except ocean. for narrowThe Sea bridgesof Japan at is either deep endand duringhas isolated periods the of lowered sea level. These access points provide potential routes for genetic the exchange of freshwater fishes on the Korean Peninsula with those on the Japanese archipelago. In the Japanese archipelago, the bottom of the Inland Sea was above sea level in glacial periods, and paleo-river systems connecting surrounding rivers (Figure2b) enabled gene flow [ 9]. Therefore, the current Inland Sea probably represented a likely dispersal route. Eastern Genes 2021, 12, x FOR PEER REVIEW 3 of 20 islands from the continent of Asia, except for narrow bridges at either end during periods of lowered sea level. These access points provide potential routes for genetic the exchange of freshwater fishes on the Korean Peninsula with those on the Japanese archipelago. In Genes 2021, 12, 303 the Japanese archipelago, the bottom of the Inland Sea was above sea level in glacial 3peri- of 18 ods, and paleo-river systems connecting surrounding rivers (Figure 2b) enabled gene flow [9]. Therefore, the current Inland Sea probably represented a likely dispersal route. East- erndispersal dispersal was was blocked blocked after after the the uplift uplift of Suzukaof Suzuka and and Nunobiki Nunobiki Mountains Mountains at aboutat about 1to 1 to1.5 1.5 Ma. Ma. SinceSince the the Japanese archipelago archipelago with with backbone mountains mountains has has few few plains, there are limitedlimited opportunitiesopportunities forfor rivers rivers flowing flowing through through different different plains plains to connect. to connect. Therefore, Therefore, gene geneflow flow among among freshwater freshwater fishes fishes is extremely is extrem low,ely aslow, salinity as salinity barriers barriers separate separate neighboring neigh- boringrivers. rivers. Dispersal Dispersal within within freshwater freshwater systems systems is prevalent, is prevalent, while while dispersal dispersal between between them themis rare, is rare, with with watersheds watersheds and oceansand oceans representing representing migration migration barriers. barriers.