Reproductive Failure of Dominant Males in the Poeciliid Fish Limia
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Proc. Nati. Acad. Sci. USA Vol. 90, pp. 7064-7068, August 1993 Population Biology Reproductive failure of dominant males in the poeciliid fish Limia perugiae determined by DNA fingerprinting (reproductive success/sexual selection/size polymorphism/social dominance/simple repetitive sequences) MANFRED SCHARTL*t, CLAUDIA ERBELDING-DENKt, SABINE H6LTER*, INDRAJIT NANDA§, MICHAEL SCHMID§, JOHANNES HORST SCHR6DERf, AND J6RG T. EPPLENI *Physiologische Chemie I, Theodor-Boveri-Institut fUr Biowissenschaften (Biozentrum) der Universitiit, Am Hubland, D-97074 Wilrzburg, Federal Republic of Germany; *Institut fUr Saugetiergenetik, GSF Forschungszentrum, Ingolstidter Landstrasse 1, D-85764 Neuherberg, Federal Republic of Germany; hnstitut fUr Humangenetik, Biozentrum der Universitit, Am Hubland, D-97074 WUrzburg, Federal Republic of Germany; and tMolekulare Humangenetik, Ruhr-Universitat, D-44780 Bochum, Federal Republic of Germany Communicated by M. Lindauer, April 22, 1993 (receivedfor review October 20, 1992) ABSTRACT Hierarchical structures among male individ- the subordinate male (15). These findings are in perfect uals in a population are frequently reflected in differences in agreement with the expectations from the hypothesis that aggressive and reproductive behavior and access to the females. large investments are rewarded by high reproductive suc- In general, social dominance requires large investments, which cess. The large and sometimes spectacularly pigmented male in turn then may have to be compensated for by high repro- morphs are regarded to be the result of sexual selection. ductive success. However, this hypothesis has so far only been Behavioral polymorphisms as well as the accompanying sufficiently tested in small mating groups (one or two males phenotypic polymorphisms are maintained or balanced by with one or two females) due to the difficulties of determining natural selection. paternity by conventional methods. DNA fmgerprinting over- Here, we use Limia perugiae, a poeciliid fish endemic to comes these problems by offering the possibility to determine the southeast of the Caribbean island Hispaniola, to study genetic relationships and mating patterns within larger groups mating patterns in relation to male polymorphism and mating [Burke, T. (1989) Trends Ecol. Evol. 4, 139-144]. We show group size. These fish inhabit freshwater biotopes-clear here that in the poeciliid fish Limia perugwe, in small mating springs as well as muddy creeks and polluted man-made groups the dominant male has a mating success of 100%, ditches. Males are polymorphic for adult size ranging from 20 whereas in larger groups its contribution to the offspring mm up to sometimes 60 mm in length. The onset of sexual unexpectedly drops to zero. maturation, which results in cessation of growth, is deter- mined by a genetic system comparable to the P locus of Sexual dimorphism is the most apparent result of sexual Xiphophorus with sex chromosomal alleles for large and selection (1, 2). The same applies for some forms of conspi- small size. However, additionally at least one autosomal cious male courtship behavior. Similarly, sexual selection is modifier locus interacts with P, thus allowing intermediate made responsible to favor the occurrence of more than one size males to appear (C.E.-D., J.H.S., I.N., M. Schmid, male morph and alternative mating behavior in certain animal J.T.E., and M. Schartl, unpublished results). Of course, populations. environmental factors modulate to a certain extent the final In the live-bearing poeciliid fish, many species are poly- size of each genotype. Females constitute a single size class morphic for male body size (3-5). Large males outcompete with a mean adult size of40 mm. Independent ofmales' social smaller ones and become dominant in the social structure of behavior, females prefer large over small males (C.E.-D., a given group (6). In at least one genus, Xiphophorus, it has J.H.S., I.N., M. Schmid, J.T.E., and M. Schartl, unpub- been conclusively shown that differences in body size result lished results). Like all other poeciliid fish species, L. peru- primarily from allelic variation of a single polymorphic Y giae does not provide parental care, and males are not chromosome-linked locus (known as P locus; refs. 4, 7-9). territorial. The sex ratio is on average one to one. The highest Large males reach sexual maturity at a much later age than rank males are marked by a very intense coloration: blue smaller ones, imposing a cost in form of an increased risk of body contrasted by a black dorsal fin and a bright yellow prereproductive mortality (5) due to predation, etc. The caudal fin with black margin. different size classes differ with respect to their sexual In the natural habitat, the social and reproductive groups behavior. Large males have a pronounced courtship behavior are larger than the two male/two female situation that could that precedes copulation attempts, whereas small males show be studied so far with the help of phenotypic markers for simple "sneaking" behavior (3, 10, 11). Additional costs of a paternal traits (e.g., see refs. 11 and 15). Simple repeat courting male include a higher risk of becoming predated oligonucleotides represent useful tools to study genetic re- because of being garish due to the more brilliant coloration lationships even in the absence of phenotypic markers (26) (12, 13). High rank males also invest the energy input within all species tested at all levels of eukaryotic organismic required to defend the hierarchy and protect females from the evolution (17). We therefore used this method to determine mating attempts of subordinate males. In female choice tests, the reproductive success of males of different social status in large males are preferred (5, 11, 14). In Xiphophorus nigren- small and large mating groups. We unexpectedly find that sis using phenotypic markers in progeny tests oftwo females with increasing size of the social groups the largest and with one large and one small male, the dominant large male dominant male becomes less successful in siring offspring. was found to be rewarded by a greater reproductive success (11). In the guppy, Poecilia reticulata, a dominant male was MATERIALS AND METHODS more successful even when the female showed preference for Experimental Animals. Our L. perugiae stocks are descen- The publication costs of this article were defrayed in part by page charge dants from fish collected in 1978 at Piedra Blanca (K stock), payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed. 7064 Downloaded by guest on September 24, 2021 Population Biology: Schartl et al. Proc. Natl. Acad. Sci. USA 90 (1993) 7065 central Dominican Republic, and at a karst spring (G stock), by rehybridization of the same gel with probes (CA)8, west Dominican Republic. Fish were kept as randomly bred (GACA)4, (GAA)6, and (TTTC)4. population stocks under standard conditions described for In a first series of experiments, one large and one small maintenance of poeciliid fish in the laboratory (18). male were tested with two females. Offspring from two Mating Experiments and Behavioral Tests. Behavioral and different broods in two independent experiments were tested mating tests with large mating groups were performed in for paternity. In one experiment, 13 of 14 animals were aquaria containing 180 liters of water with a sandy bed and attributable to the large dominant male and one was of containing several plants and hiding places to simulate the uncertain paternity. In the second case, all 12 F1 fish tested habitat found in nature (ref. 19; M. Meyer, personal com- were unequivocally offspring of the a male. munication) at a 12-h day/12-h night artificial light cycle. For In the second set ofexperiments, four males ranging in size the social groups, males and females from both K and G from 25 mm to 49 mm were assembled with four or five stocks were mixed. Exclusively young males and juvenile juvenile, virgin females. In three trials within a few days, the virgin females were assembled for the mating experiments to male fish established a size-dependent ranking that remained allow the social structure to establish before successful stable throughout the duration of the experiment. DNA mating attempts could occur. For the two males/two females fingerprinting ofa representative number ofoffspring (Fig. 2) situation, 30-liter tanks were used with otherwise the same revealed that most females had contributed to the offspring conditions. Newborn fish were collected from the experi- generation and that generally individual broods were of mental tank and raised separately. After termination of the mixed paternity. In the first mating group, all offspring tested mating were from one of the subordinate males. In the second and experiments (3-4 months), females were isolated, and third group, paternity was assigned to both the (3 and 'y male. their next brood was raised separately. The male fish are In all cases, the smallest and most subordinate male never referred to as a, 3, 'y, and co in decreasing order ofsocial rank. had offspring. This is in agreement with its exclusively DNA Fingerprinting. DNA was extracted from all adult fish defensive behavior. Surprisingly, none of the progeny were used in the mating experiments and from a representative fathered by the dominant male (Table 1). After experiments number of randomly selected offspring as described (20). 2 and 3, full fertility of the a males was confirmed by mating Determination of paternal and maternal relationships by them without competition to virgin females. In the fourth simple repeat oligonucleotide fingerprinting was performed mating group, males were assembled that did not establish a as described (21). pronounced hierarchy, although size differences allowed some ranking. The lowest rank male did not exhibit hiding RESULTS and the a male was far less aggressive than in the three other After evaluating different restriction enzyme/probe combi- mating groups.