TROPHIC DIFFERENTIATION in <I>ILYODON</I>

Evolution, 34(2), 1980, pp. 259-270 TROPHIC DIFFERENTIATION IN ILYODON, A GENUS OF STREAM-DWELLING GOODEID FISHES: SPECIATION VERSUS ECOLOGICAL POLYMORPHISM BRUCE J. TURNER' AND DANIEL J. GROSSE Museum of Zoology, University of Michigan, Ann Arbor, Michigan 48109 Received March 15, 1979. Revised September 10, 1979 An impressive diversity of trophic ad tected two trophically divergent, sympat aptations is a hallmark of teleostean fish ric clones of the triploid unisexual fish es, and has been a characteristic of their species Poeciliopsis 2-monacha-lucida. evolution that dates from their first The clones, though obviously closely re appearance in the fossil record. Students lated, were differentiated in dental mor of this diversity have usually regarded a phology and feeding behavior. particular suite of functionally related The implications of the discovery of dis trophic specializations as attributes of a continuous trophic polymorphisms in sin given species that adapt it to a particular gle populations are far-reaching. From the ecological niche and tend to exclude it perspective of ichthyology, the existence from other niches. Generally, though al of such polymorphisms (involving well lowance is made for developmental vari defined "taxonomic" characters) suggests ation or sexual dimorphism, a species has that the number of biological species in been presumed to have only one set (or a volved in several extreme radiations of narrow range) of trophic adaptations. It trophic diversity, most notably those of has been thought extremely unlikely for cichlids in the African Rift lakes (Fryer contemporaneous adult members of the and Iles, 1972) and of cyprinids in Lake same Mendelian population to possess Lanao (Myers, 1960), may have been se radically different (and mutually exclu riously overestimated by morphological sive) arrays of trophic features. Thus, es inferences (see also Kornfield, 1978). The pecially at or near the species level, ich nature of the radiations themselves, as thyologists have tended to equate trophic well as the systematic utility of trophic differentiation with systematic diver characters in general, may have to be gence. The generality of this relationship reevaluated. From the perspective of ecol has recently been seriously challenged. ogy, trophic polymorphism implies that Sage and Selander (1975) have demon "a single species occupies niches that are strated that three trophically specialized as distinctly different as is usually the case sympatric cichlids (Cichlasoma) in the among validly different species" (Hutch Cuatro Cienagas basin of Coahuila, Mex inson, 1978, p. 179), and leads to a host ico, a molluskivore (with molariform pha of questions concerning the ecological re ryngeal teeth and a short gut), an algal lationships of the trophic morphs. From detritus feeder (papilliform pharyngeal the perspective of evolutionary genetics, the teeth and a long gut) and a piscivore-all discontinous trophic variation may well be previously thought to be distinct species the type of niche-specific polymorphism (Taylor and Minckley, 1966)-exhibited that Maynard Smith (1966) and others coordinate geographic variation at several have regarded as a fundamental requisite allozyme loci, and were therefore most for sympatric speciation. likely conspecific. Vrijenhoek (1978) de- The only other known case of trophic polymorphism in teleosts is that postulat , Present address: Department of Biology, Virgin ed in species of the characoid genus Sac ia Polytechnic Institute & State University, Blacks codon by Roberts (1974): up to four dental burg, Virginia 24061. morphs occur in what appear to be con 259 260 B. J. TURNER AND D. ]. GROSSE FIG. 1. Lateral views of Ilyodon specimens from "dichotomous" populations, males above, females below, in each. a. Type A, Rio Tuxpan drainage (Rio "Terrero"; UMMZ 191681, male is 56 mm Standard Length). b. Type B, collected simultaneously with "A" (UMMZ 191680, male is 57.5 mm S.L.). c. Type A, Rio Armeria drainage (Ilyodonfurcidens; Rio de Comala; UMMZ 189595, male is 59 mm S.L.). d. Type B (Ilyodon xantusi); collected simultaneously with "C" (UMMZ 189594, male is 64 mm S.L.). specific population samples of these algal rant of the Mexican plateau into the Pa grazing fishes from the mountain streams cific Ocean. of Panama and northwestern South Amer The llyodon populations of certain trib ica. Unfortunately, genetic or other bio utaries of two river drainages, the Rio logical data from the Saccodon dental Armeria and Rio Tuxpan (=Rio Coa morphs are entirely lacking. huayana), can be divided into two very In this paper we present biochemical distinctive morphological (presumably genetic analyses of two sets of sympatric, trophic) "types" (Figs. 2 and 3): trophically specialized, putative species of a little-known Mexican fish genus, Ily Type "A": The head is tapered, with rel odon. This genus is a member of the vi atively small jaws; the gape of viparous fish family Goodeidae, a family the mouth is conspicuously of less than 40 species of cyprinodontoid lateral, and the jaw teeth (bi fishes with unique reproductive adapta fid in both types) tend to be tions (Miller and Fitzsimons, 1971). The short and organized into two family is essentially endemic to the Mex obvious rows on the premax ican plateau, where it has undergone an illae (usually one on the den adaptive radiation into habitats and tary bones). trophic niches more usually occupied by Type "B": The head is very blunt with members of several other fish families. Il relatively massive jaws; the yodon species are small (usually less than gape of the mouth is almost 120 mm total length), laterally com completely transverse (fron pressed, minnow-like fishes (Fig. 1). Un tal), and the jaw teeth tend to like nearly all other goodeids (most of be elongate, posteriorly exca which are typically lake dwellers), llyodon vated, fewer in number, and are fluviatile, like Saccodon, and are al in larger specimens organized most exclusively confined to the montane in but a single row on both rivers that flow off the southwest quad- jaws. TROPHIC DIFFERENTIATION IN ILYODON 261 a c b FIG. 2. Enlarged frontal views of specimens shown in Fig. 1; data as in Fig. 1. Note the wider, more massive jaws of the "B" types in both river systems. The morphology of type"A" suggests that types in the R. Armeria as I lyodon fur of an insectivore or planktivore, that of cidens and Balsadichthys xantusi, respec "B" a substrate feeder, possibly a har tively; "Balsadichthys" was vacated in fa vester of lithophilic algae or small ani vor of Ilyodon by Miller and Fitzsimons mals; however, no detailed dietary data (1971). are yet available. The two trophic types The two trophic types are readily dif breed true in the laboratory, and develop ferentiated by eye (above a size of about their distinctive phenotypes when reared 35 mm in total length), but relative mouth on identical diets. They thus probably do width (ratio of premaxillary width to head not represent "ecophenotypic" or devel length) provides a convenient discrimina opmental modifications of the same array tion (Hubbs and Turner, 1939). The fre of genotypes (see discussion by Kornfield quency distribution of the ratio is essen and Koehn, 1975). With the exception of tially bimodal in samples of populations a small difference in adult male color pat that contain both types (Fig. 3). tern in the R. Armeria (see below), the The two river drainages also contain morphological differences between the Ilyodon populations that are not dichot types are all plausibly associated with di omous, but rather highly variable in vergent trophic adaptations. trophic features. Those in the R. Tuxpan The trophic types are quite distinctive, are otherwise virtually identical to the di and, if presented with Figure 2 few ich chotomous populations. The frequency thyologists (ourselves initially included) distributions of the mouth width:head would hesitate to suggest that they are length ratio in these populations are not different species. In the last major taxo bimodal (Fig. 3C and D) and means are nomic revision of the family, Hubbs and near the antimode of the dichotomous Turner (1939) recognized the A and B populations. In the R. Tuxpan drainage, 262 B. J. TURNER AND D. J. GROSSE R. TUXPAN -+- lations are encountered almost exclusively in high-gradient tributaries with rock and TRIBUTARY 16 KM N boulder-strewn substrates and abundant U A PIHUAMQ("RIO TERRERO ) riffles. The non-dichotomous populations are usually found in low-gradient habitats with pebble or silt substrates. When first TRIBUTARY 8 KM N observed, in collections from the R. Ar PIHUAMO ("RIO TERRERO"?J meria, Ilyodon of intermediate phenotype were regarded as interspecific (and inter -+ generic) hybrids (Hubbs and Turner, TRIBUTARY AT TECALITLaN 1939). c Knowledge of the relationships of the trophic types in the dichotomous popula -+- SAN RAFAEL BRIDGE tions is obviously central to understanding the evolution of trophic diversity in Ily D odon. Do they represent discrete gene pools, or are they components of the same + R. ARMERIA Mendelian population? In this paper we 20 attempt to answer this question by com 15 R. DE COMALA parison of polymorphic allozyme loci in AT COMALA the trophic types in two dichotomous pop E 10 ulations, one from each of the river streams. The data suggest that at least one of these sympatric "species pairs" may in .50 .55 .60 fact be a single Mendelian population with MOUTH WIDTH / HEAD LENGTH discrete trophic morphs. FIG. 3. Histograms of the frequency distribu tions of relative mouth widths (mouth width/head MATERIALS AND METHODS length) in five Ilyodon samples. Solid black squares Specimens.-Samples were taken by represent individuals scored as Type A by eye, open white squares represent those scored as Type B. poisoning with emulsified rotenone at the Striped (gray) boxes represent individuals which following localities: could not be reliably scored by eye.

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