TRANSACTIONS E AMERICATH F O N FISHERIES SOCIETY Volume 122 January 1993 Number 1 Transactions of the American Fisheries Society 122:1-33. 1993 Copyrigh© thy tb e American Fisheries Society 1993 Phytogen Pacifie th f yo c Trout Salmond san s (Oncorhynchus) and Genera of the Family Salmonidae . STEARLEYF . R '. SMITANR . DG H Museum of Paleontology and Museum of Zoology University of Michigan. Ann Arbor. Michigan 48109. USA Abstract.— Seven genera—Brachymystax. Acantholingua. Salmothymus, Hucho. Salvelinus. Sal- mo, and Oncorhynchus—make up the living Salmoninae. Relationships of 33 extant and 4 fossil salmonid specie subspecied san s were studie basie th f 11 so n d9o characters analyze parsimony db y algorithms. Twelve equally parsimonious trees each requirin step3 g25 s were calculated. Mono- phyly of recognized genera is consistent with all 12 estimates. The earliest branch of the family Salmonidae is the subfamily Coregoninae. Its sister group is the clade including the Thymallinae and Salmoninae. Within the Salmoninae, Eosalmo, from the Eocene of British Columbia, is the sister group of all living genera, as previously shown by Mark Wilson. The living Asian species Brachymystax lenok is the sister species of all other living Salmoninae, as documented by Carroll Norden. Three species of archaic trouts from the Mediterranean area—Acantholingua ohridana. Salmothymus obtusirostris, and Salmothymus (Platysalmo) platycephalus—branch off after Brachymystax but before diversification of all other salmonines. Platysalmo platycephalus Behnke sistee isth r species of Salmothymus obtusirostris places i d Salmothymus.n di an clade Th e beyond the archaic trouts includes four genera in two clades: (1) Hucho plus Salvelinus and (2) Salmo plus Oncorhynchus. Atlantie Th c trout salmond san monophyleti a e sar c group, e Salmo.th d an Pacific trouts and salmons are a monophyletic group, Oncorhynchus. The terms "trout" and "salmon" refer roughl lifo yt e history modesphylogenetio t t no , c relationships. Morphological mitochondriad an l DNA data disagree regardin relationshie gth p of Oncorhynchus clarki (cutthroat trout Oncorhynchuso )t mykiss (rainbow, California golden redband an , d relation e troutsth d )an - shi Oncorhynchusf po gorbuscha (pink salmon Oncorhynchuso t ) keta (chum salmon). Parsimony analysis suggests that Oncorhynchus Pacifie mykiss sistee th th f . o clarki,s cri O salmon f o t no , thoug mykiss. clarki. O h O d an hybridize. Oncorhynchus gorbuscha sistee th s ri specie . nerka0 f so (sockeye salmon), not of keta. though O. gorbuscha and O. keta hybridize. Mitochondrial DNA is interprete s havina d g been transferre introgressioy db n betwee . gorbuschanO . keta,O d an providing misleading evidenc relationshipf eo . Fossil specie Oncorhynchusf so documen minia t - millio6 f o mu e nmmodere ag year th r sfo n specie Pacifif o s c trout salmonsd san . The family Salmonidae includes three subfam- vica, huchen, taimen, chars, trouts d salman , - ilies—Coregoninae (whitefishes), Thymallinae ons)—widely distributed in the northern hemi- (graylings), and Salmoninae (lenok, mekous, bel- sphere (Norden 1961). Ther strons i e g evidence that eac thesf ho monophyletia s ei c clade nata , - 1 Present address: Department of Geology, Geogra- ural group tha tdescendant e containth f o l sal f o s phy, and Environmental Studies, Calvin College, 3201 its most recent common ancestor Salmonie Th . - Burton Avenue, Grand Rapids, Michigan 49546, USA basae ar .le Euteleosteda i relateEsocoideie th o dt , 1 STEARLEY AND SMITH Ostariophysi, Argentinoidei, and Osmeroidei fishes, such as osmerids, now placed outside the (Lauder and Liem 1983; Fink 1984; Begle 1991). family Salmonidae). centurieDurino tw e gth s since Previous salmonid phylogenies (e.g., Norden 1961; Linnaeus's classification, ichthyologists have Wilson 1974; Kendall and Behnke 1984; Sanford thoroughly documente classified dan d salmonine 1990) have interpreted the Salmoninae and Thy- diversity. Following is a brief summary of the tax- mallina s sisteea r group f eaco s e h th othe d an r onomic histories of three salmonine assemblages: Coregoninae as the sister group of the clade in- (1) the four genera of morphologically plesiomor- cluding those two (Figure la, b, c). phic "archaic trouts, huchee th ) "(2 n (Hucho)d an subfamile Th y Salmoninae comprises between chars (Salvelinus), more th ) e (3 derive d an d salm- fivd ninan e e extant genera (Figure 1) containing troutd an Salmon s si on Oncorhynchus.d an approximatel specie0 y3 s (Norden 1961; Behnke 1968; Kendall and Behnke 1984). The best known Archaic Trouts genera are Hucho, Salvelinus, Salmo, and Onco- At least four species of archaic trouts in Brachy- rhynchus, which are relatively advanced salmonid mystax, Salmothymus, Acantholingua, Pla-d an fishes. Four other laxa—Brachymystax. Platysal- tysalmo are native to Siberia, China, Korea, Ar- mo, Salmothymus, and Acantholingua—are mor- menia drainaged an ,northease th n so t periphery phologically primitive and their relationships have of the Mediterranean Sea from Dalmatia to Tur- been problematic. The last three are often includ- key. They possess short, broad maxilla shord ean t Salmo.n i d e additionn I , four fossil generd aan dentaries with high coronoid processes, and they several fossil species belongin extano gt t genera have small teeth. The phylogenetic relationships have been recognized. Withou phylogena t y based of these archaic trouts have bee nproblea - mbe on broad evidence fro l speciesmal directioe th , n cause they share primitive character- s ge wit e hth of evolution and the positions of the fossils and nus Salmo. Norden (1961) recognized that problematic taxa relative to the more advanced Brachymystax is morphologically and phyloge- genera canno knowne tb relationshipe .Th charf so s netically intermediate between Thymallusd an (Salvelinus) to other salmonines are also crucial more derived salmonines, base severan do l fea- classificatioe th o t f troutno salmonsd san . Some tures. However, other systematists have placed systematists (e.g., Norden 1961) have considered Brachymystax as the sister group of Hucho, be- Salvelinus sistee th s ra lineag clada f eo e including cause they share a unique vomerine tooth pattern Salmo d Oncorhynchus,an whereas others (e.g., (discussed below). Kendal Behnkd an l e 1984) have placed Salvelinus Salmothymus is sometimes considered to in- close Huchoo rt Brachymystax.d an clude two species, 5. obtusirostris (Heckel), the Although salmonid biologists agree that Atlan- Dalmation trout or "mekous," and S. (Acantho- tic salmon Salmo salar and brown trout Salmo lingua) ohridanus (Steindachner), the "belvica," trutta are closely related to Pacific trouts and endemic to Lake Ohrid in Yugoslavia. Behnke salmons, they have disagreed about the classifi- (1968:10) noted: "although vital to any compre- catio f Pacifino c trouts. Regan (1914 d Vlaan ) - hensive phylogenetic study of salmonid fishes, the dykov (1963) drew attention to the closer rela- statu Salmothymusf so neves ha r been firml- yes tionshi f Pacifio p c trout o Pacifit s c salmons tablished." Steindachner's classifications of Sal- (Oncorhynchus) tha Atlantio nt c trou salmod tan n mothymus obtusirostris demonstrate the ambigu- (Salmo). Traditionally, however, Pacific trouts ity indicate morphologys it y db firse h : t classified have been classified in Salmo, thus making Salmo the mekous as a grayling, Thymallus microlepis an unnatural group—paraphyletic—because it does (1874) t latebu , r place Salmon i t di (Steindachner no s descendantt it includ f o l al e s (Smitd an h 1882). Berg (1908:505) calle Salmothymust di - ob Stearley 1989). In the present paper, the relation- tusirostris. remarking that its features were inter- ships of the species of Pacific trouts and salmons mediate between Brachymystax and Salmo: "Sie eaco t h othe treatee contexe r ar phy e th th n d i -f to bildet eine besondere Gattung, welch n Bineei - logen l fossi al Recend f yan lo t gener f salmonao - deglied zwische eben nde n genannten Gattungen ines. [i.e., Salmo and Brachymystax] darstellt." Had- zisce (1961) first recognize fundamentae dth l dif- Histor Salmof yo Troud nan t Classification ferences between obtusirostris ohridanusd an d an Salmo, as proposed by Linnaeus in 1758, in- allocated the two species to two monotypic gen- cluded all salmonines then known, as well as thy- era— Salmothymus obtusirostris and Acantholin- mallines and coregonines (and some groups of gua ohridana. Behnke (1968) considered Sal- SALMONID PHYLOGENY FIGURE 1 .—The major phylogenetic hypotheses regarding the Salmonidae (rearranged to comparable format): (a) Norden (1961) Wilso) (b , n (1974) Kendal) (c , Behnkd an l e (1984) Dorofeyev) (d , a (1989) daggee Th . r indicatesa fossil taxon; dotted lines indicate uncertainty. mothymus Acantholinguad an subgenere b o t f ao Huchen Charsand Salmo. Svetovidov (1975) placed Acantholingua ohridana in Sal mothymus, a classification that has huchee Th describes nwa Linnaeuy db s (1758) been widely followed. as Salmo hucho and placed in the subgenus Hucho Behnke (1968) described another species of ar- by Gunther (1866). Jordan and Snyder (1902) el- chaic trout, Salmo (Platysalmo) platycephalus, evated Hucho to generic rank and described a sec- from Turkey. He saw evidence that Platysalmo, ond species, H. perryi. Vladykov (1963) created like Salmothymus and Acantholingua, had di- the subgenus Parahucho for Hucho perryi. Lindsey verged from European Salmo long before differ- (1964) called attention to broad similarities be- entiation of modern Salmo salarand S. trutta had tween Hucho Salvelinus.d an huchet Bu n wer- ere occurred classifiee h t bu , d the Salmo.mn i Simi- garde closs da e relatives of Brachymystax Shay b - larly, "Salmo" ischan from Armenia and "Sal- poshnikova(1968, 1975), Holdik (1982a, 1982b), " carpiomo fro mArchaie b Italy yma c trout- sre d Holcian t ale k . (1988). Kendal d Behnkan l e late o Salmothymust d obtusirostris. S d an (1984) treated Brachymystax plus Hucho clada s a e platycephalus.