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Historical and Contemporary Diversity of Galaxiids in South America: Biogeographic and Phylogenetic Perspectives

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Historical and Contemporary Diversity of Galaxiids in South America: Biogeographic and Phylogenetic Perspectives diversity Review Historical and Contemporary Diversity of Galaxiids in South America: Biogeographic and Phylogenetic Perspectives Iván Vera-Escalona 1,2,* , M. Lisette Delgado 3 , Evelyn Habit 4 and Daniel E. Ruzzante 3,* 1 Departamento de Ecología, Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Casilla 297, Concepción 4090541, Chile 2 CIBAS, Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Casilla 297, Concepción 4090541, Chile 3 Department of Biology, Dalhousie University, Halifax, NS B3H4R2, Canada; [email protected] 4 Departamento de Sistemas Acuáticos, Facultad de Ciencias Ambientales y Centro EULA, Universidad de Concepción, Concepción 4070386, Chile; [email protected] * Correspondence: [email protected] (I.V.-E.); [email protected] (D.E.R.) Received: 27 May 2020; Accepted: 28 July 2020; Published: 5 August 2020 Abstract: Galaxiid fishes from South America are represented by three genera (Aplochiton, Brachygalaxias and Galaxias) and eight species. Their genetic patterns have been studied over the last two decades to disentangle how historical and contemporary processes influenced their biogeographic distribution and phylogeographic patterns. Here we review and synthesize this body of work. Phylogeographic approaches reveal the important role played by orogeny and the expansion/melting of glacial ice during the Quaternary. Populations retreated to glacial refugia during glacial times and some systems experienced drainage reversals from the Atlantic to the Pacific following deglaciation. Although most species expanded their populations and increased their genetic diversity during the Holocene, the introduction of salmonids and the construction of dams are likely to lead to a decline in genetic diversity for at least some species. An improvement in our understanding of the processes that influenced historical and contemporary diversity patterns among galaxiid and other native fishes in South America is necessary for addressing the cumulative and synergistic impacts of human activity on this unique freshwater fauna. Keywords: Galaxiidae; fish; Patagonia; genetics; phylogeny 1. Introduction Galaxiid fishes (Galaxiidae) in South America are represented by three genera and eight species (Galaxias maculatus, G. platei, G. globiceps, Aplochiton zebra, A. marinus, A. taeniatus, Brachygalaxias bullocki, and B. gothei) distributed throughout the Southern Cone in continental Patagonia on both sides of the Andes as well as in Tierra del Fuego and the Falkland/Malvinas islands ([1]; Figure1A). The various species in the group differ in their life histories, and though their respective ranges overlap, they differ substantially in their distributions. Galaxias maculatus and G. platei are the two most widespread species in the group and their distributions coincide with the area covered by the icecap during the Last Glacial Maximum (LGM), including the area west of the icecap north of Lat 42◦ S where the ice coverage did not reach the sea (Figure1B). One di fference between these two species, however, is that G. maculatus (but not G. platei) is present in estuarine and coastal areas as indicated below. The other species in the group are also found within the area covered by the LGM icecap, but they tend to be present less frequently and in smaller numbers than G. maculatus [2]. Diversity 2020, 12, 304; doi:10.3390/d12080304 www.mdpi.com/journal/diversity Diversity 2020, 12, x FOR PEER REVIEW 2 of 14 Diversityindicated2020 below., 12, 304 The other species in the group are also found within the area covered by the2 LGM of 14 icecap, but they tend to be present less frequently and in smaller numbers than G. maculatus [2]. FigureFigure 1.1. (A(A) )Southern Southern hemisphere hemisphere map map including including GalaxiasGalaxias (in (inyellow), yellow), AplochitonAplochiton (in red),(in red), and andBrachygalaxiasBrachygalaxias (in light(in light blue) blue) range range species species from from South South America America and and G. G.maculatus maculatus rangerange outside outside of ofSouth South America America (in (in green). green). West West Wind Wind Drift Drift in magenta in magenta arrows. arrows. (B) South (B) South America America zoomed zoomed map mapwith withschematic schematic main main landscape landscape changes changes in Patagonia in Patagonia and presumed and presumed direction direction of retre ofat retreatto glacial to glacialrefugia refugia(marked (marked with arrows) with arrows) explaining explaining the principal the principal phylogeographic phylogeographic patterns patterns of galaxiid of galaxiid species species during duringglacial glacialtimes. Approximate times. Approximate glacial glacialice cover ice at cover the time at the of time the Last of the Glacial Last Glacial Maximum Maximum (LGM) (LGM)shown shownin grey. in Exposed grey. Exposed area of Patagonia area of Patagonia during the during LGM the(in dark LGM grey) (in darkdue to grey) sea level due todrop sea (180 level m) drop (See (180[3,4] m)). (SeePaleocoast [3,4]). Paleocoastduring the during Last theGlacial Last GlacialMaximum Maximum based based on onfree free data data available available fromfrom https:https://crc806db.uni//crc806db.uni-koeln.de-koeln.de/layer/show/327/./layer/show/327/. GalaxiasGalaxias maculatus,maculatus, thethe mostmost widelywidely distributeddistributed speciesspecies inin thethe groupgroup exhibitsexhibits bothboth freshwaterfreshwater residentresident (whether(whether landlockedlandlocked oror not)not) as as well well as as diadromous diadromous populations. populations. Diadromous Diadromous populationspopulations inhabitinhabit estuarineestuarine andand coastalcoastal marinemarine habitatshabitats alongalong thethe PacificPacific coastcoast [5[5]],, thethe AtlanticAtlantic coastcoast inin southernmostsouthernmost PatagoniaPatagonia [[6]6] asas wellwell asas thethe island of Tierra del Fuego [7] [7].. GalaxiasGalaxias maculatus maculatus hashas a arelatively relatively short short generation generation time; time; individuals individuals usually usually reach reach maturity maturity before before their their first firstyearyear of life, of with life, withthe most the most common common cohort cohort among among reproductively reproductively mature mature individuals individuals often being often the being 1+ thecohort. 1+ cohort. Adults Adults> 3 years> 3 of years age are of age rarely are found rarely found[8]. Freshwater [8]. Freshwater resident resident G. maculatusG. maculatus lay theirlay eggs their in eggs littoral in littoral zones zonesof lakes of lakesand andon riverine on riverine floodplains floodplains with with abundant abundant vegetation, vegetation, exhibiting exhibiting a a repetitive spawningspawning strategystrategy [ [88––1010]].. AfterAfter hatching,hatching, larvaelarvae undertakeundertake significantsignificant habitathabitat shifts,shifts, migratingmigrating fromfrom thethe littorallittoral toto thethe limneticlimnetic zonezone [11[11]].. InIn estuaries,estuaries, G.G. maculatusmaculatus spawnsspawns onon thethe toptop ofof floodedflooded grassgrass flatsflats afterafter thethe highesthighest high-water high-water spring spring tide tide [ 12[12]]..As As thethe tidetide recedes,recedes,the theeggs eggsare are washed washed down down to to the the bases bases of of the the grassgrass clumpsclumps where where the the highhigh humidityhumidity ofof thethe vegetationvegetation protectsprotects themthem fromfrom desiccationdesiccation until until thethe nextnext springspring tides tides a a fortnight fortnight later later [13 [13]]. Larvae. Larvae are are subsequently subsequently washed washed out to out sea to where sea where the juveniles the juveniles spend approximatelyspend approximately six months six months before returningbefore returning to freshwater. to freshwater. Hatching Hatching during during flood events flood events may favor may larvalfavor survivallarval survival as turbid as flowsturbid likely flows provide likely coverprovide as larvaecover as migrate larvae out migrate to sea out [14]. toGalaxias sea [14] maculatus. Galaxias formmaculatus large form shoals large that shoals swim that during swim the during day; they the day tend; they to feed tend on to zooplankton feed on zooplankton in lakes and in lakes benthic and macroinvertebratesbenthic macroinvertebrates in rivers, in floodplains, rivers, floodplains, and estuaries. and estuaries. Lacustrine Lacustrine individuals individuals tend to havetend ato more have fusiforma more body,fusiform narrower body, heads,narrower and heads, larger eyesand thanlarger riverine eyes individualsthan riverine [15 individuals]. Similar morphological [15]. Similar divergencemorphological patterns divergence have recently patterns been have described recently forbeen other described galaxiid for species other galaxiid inhabiting species lentic inhabiting and lotic environmentslentic and lotic [16 environments]. [16]. GalaxiasGalaxias plateiplatei,, a strictly strictly freshwater freshwater species species largely largely restricted restricted to to lacustrine lacustrine environments, environments, is isdistributed distributed throughout throughout Andean Andean Patagonia Patagonia and and Tierra Tierra del Fuego. Their juveniles are mostmost commonlycommonly foundfound inin thethe shallowshallow littorallittoral zonezone ofof lakes,lakes, whilewhile largelarge adultadult individualsindividuals inhabitinginhabiting multispeciesmultispecies communitiescommunities areare mostmost commoncommon inin deepdeep
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