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Dissolution of Sexual Signal Complexes in a Hybrid Zone Between the Swordtails Xiphophorus Birchmanni and Xiphophorus Malinche (Poeciliidae)

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Dissolution of Sexual Signal Complexes in a Hybrid Zone Between the Swordtails Xiphophorus Birchmanni and Xiphophorus Malinche (Poeciliidae) COPEIA Friday Feb 21 2003 06:25 PM cope 03_210 Mp_299 Allen Press x DTPro System File # 10TQ Copeia, 2003(2), pp. 299±307 Dissolution of Sexual Signal Complexes in a Hybrid Zone between the Swordtails Xiphophorus birchmanni and Xiphophorus malinche (Poeciliidae) GIL G. ROSENTHAL,XOCHITL F. DE LA ROSA REYNA,STEVEN KAZIANIS, MATTHEW J. STEPHENS,DONALD C. MORIZOT,MICHAEL J. RYAN, AND FRANCISCO J. GARCIÂADELEOÂ N The evolution of sexual signaling systems is in¯uenced by natural and sexual selection acting on complex interactions among traits. Natural hybrid zones are ex- cellent systems for assessing ®tness effects on sexual phenotypes. Most documented hybrid zones, however, show little variation in sexual signals. A hybrid zone between the swordtails Xiphophorus birchmanni and Xiphophorus malinche is characterized by numerous recombinants for male sexual traits. Analyses of geographic variation in morphological and isozyme traits in the RõÂo Calnali, Hidalgo, Mexico, reveal an upstream-to-downstream gradient from X. malinche-toX. birchmanni-type traits. A second hybrid zone, likely isolated from the R. Calnali, occurs in the nearby Arroyo Pochutla. Although the presumed female preference for swords predicts the intro- gression of swords from X. malinche-like populations into hybrid populations, the opposite pattern was observed. Swords are reduced in populations otherwise char- acterized by X. malinche traits. Sexually dimorphic traits were poorly correlated with- in individuals, indicating that sexual selection does not act against recombinant phe- notypes. Hybrid males also exhibit trait values outside the range of parental varia- tion. These patterns are consistent with predictions that females are permissive, preferring generally conspicuous males without attending to speci®c features. ONSPICUOUS sexual signals often involve nisms underlying trait-preference associations. C suites of traits that interact in complex Most studies to date on sexual signals in hybrid ways to in¯uence receiver perception. Both zones, however, have focused on variation in multivariate statistical analysis (Endler and Hou- one or a few, functionally related, signal vari- de, 1995) and experimental manipulation of ables (e.g., Sanderson et al., 1992; Parsons et al., phenotypes (Sinervo and Basolo, 1996) have 1993; McDonald et al., 2001). taken a combinatorial approach, evaluating The swordtails Xiphophorus birchmanni (Fig. multiple trait combinations to ascertain their ef- 1A) and Xiphophorus malinche (Fig. 1B) both in- fect on female mating preferences. Yet con- habit shallow, rocky streams. The two species trolled studies such as these can only suggest are members of the monophyletic RõÂo Panuco the maximum theoretical evolutionary effect of basin, or northern, species group of swordtails. sexual selection, since other aspects of the trait The phylogenetic hypotheses differ as to the re- complex being analyzed are unconstrained by lationship of the two species. Hypotheses based the biology of the system and by their ®tness on behavioral, morphological, and allozyme consequences in nature. traits (Rauchenberger et al., 1990), RAPDs (Bo- Natural hybrids, however, offer the opportu- rowsky et al., 1995), and a combined analysis of nity to measure the overall evolutionary effects these (Marcus and McCune, 1999) place the of natural and sexual selection on trait com- two as sister species. The strict and semistrict plexes. Traits can often interact in surprising consensus trees in Morris et al.'s (2001) allo- ways (e.g., Nijhout and Emlen, 1998); hence zyme study place both species in a polytomy natural hybrids can also indicate the range of with Xiphophorus cortezi. Meyer et al.'s (1994) hy- trait combinations that are genetically and de- pothesis, based on DNA sequence data, shows velopmentally possible. This requires a hybrid weak support for pairings of X. birchmanni with zone involving parental species with pro- Xiphophorus pygmaeus and X. malinche with X. cor- nounced, measurable differences in sexually se- tezi. Marcus and McCune's (1999) total-evidence lected traits. Documenting the distribution of tree based on morphological, behavioral, recombinant phenotypes in a hybrid zone per- RAPD, and sequence data shows weak support mits one to re®ne hypotheses as to how multi- for X. birchmanni at the base of the RõÂo Panuco ple-trait signals are maintained in nature and basin swordtails, and pairs X. malinche and X. can provide insights into the genetic mecha- cortezi. q 2003 by the American Society of Ichthyologists and Herpetologists COPEIA Friday Feb 21 2003 06:25 PM cope 03_210 Mp_300 Allen Press x DTPro System File # 10TQ 300 COPEIA, 2003, NO. 2 males also express an irregular array of oval, ¯anking vertical bars. Xiphophorus birchmanni,in contrast, lack swords or bear short swords, have an elongate dorsal ®n, and express vertical bars in a regular series (Rauchenberger et al., 1990). In addition to sexually dimorphic traits, the spe- cies are distinguished by the number of rows of middorsal spots (3±4 in X. malinche vs 1±2 in X. birchmanni; Rauchenberger et al., 1990) and by different isozyme alleles at two loci (see below). Females in other swordtail species choose males on the basis of swords (Basolo, 1990, 1995a; Rosenthal and Evans, 1998), vertical bars (Morris et al., 1995), and body size (Ryan and Wagner, 1987; Ryan et al., 1990; Morris et al., 1996) . The dorsal ®n has been implicated in mate choice in another poeciliid, the sail®n molly Poecilia latipinna (Ptacek, 1998). In male X. birchmanni, X. malinche and other northern swordtails, the dorsal ®n is only fully erect dur- ing courtship and agonistic interactions, strong- ly suggesting that it plays a role in signaling. In addition, the species differ in the expression of two independent, Mendelian melanophore pig- ment pattern polymorphisms: Caudal blotch (Cb) is polymorphic in X. malinche and absent in X. birchmanni, whereas the converse is true for Spot- ted caudal (Sc [Rauchenberger et al., 1990]). The production of viable hybrid Xiphophorus is a routine laboratory practice; many species hybridize readily when housed in the same aquarium (Kazianis et al., 1996). Hybrid genetic crosses are especially valuable to the cancer re- search community, since melanistic pigment patterns derived from crosses of parental stocks are often phenotypically enhanced, resulting in Fig. 1. Representative males from parental and hy- extreme melanization and melanoma formation brid populations. (A) Xiphophorus birchmanni collected (Schartl, 1995; Fig. 1C). Nevertheless, there are at Huiznopal, RõÂo Conzintla. Note nuchal hump. (B) no well-documented cases of natural hybridiza- Xiphophorus malinche from RõÂo Claro stock. (C) hybrid tion in Xiphophorus (but for a possible instance, from Calnali-low. Spotted caudal macromelanophore see Rosen, 1979). We report here genetic and pattern, diagnostic of X. birchmanni, shows evidence morphological evidence of a hybrid zone in the of melanosis. The sword is diagnostic of X. malinche, RõÂo Calnali, Hidalgo, Mexico, characterized by whereas the regular vertical bars are diagnostic of X. numerous individuals with recombinant suites birchmanni. (D) Hybrid collected at Calnali-mid. Note of sexually dimorphic traits. irregular bars, diagnostic of X. malinche, and deep body and reduced sword, diagnostic of X. birchmanni. MATERIALS AND METHODS Xiphophorus malinche has a strictly highland Isozyme electrophoresis.ÐFish were collected by distribution, whereas X. birchmanni is generally seine and dip net in March 1999 from three sites found at lower elevation, in warmer water on the RõÂo Calnali, Hidalgo, Mexico (Fig. 2): Cal- (Rauchenberger et al., 1990). The species are nali-high (208539540N, 988379390W [GPS map da- characterized by dramatically different com- tum: WGS 84]), Calnali-mid (208539340N, 988369 plexes of sexually dimorphic traits. Male X. mal- 360W), and Calnali-low (208559260N, 988349350 inche are ``typical'' northern swordtails, with a W). We sampled apparent hybrids from a single pronounced, pigmented elongation of the low- locality on the nearby Arroyo Pochutla (208519 er rays of the caudal ®n (``sword'') and a mod- 390N, 988349230W). We also sampled allopatric erately sized dorsal ®n. Xiphophorus malinche populations of the two parent species. Xiphopho- COPEIA Friday Feb 21 2003 06:25 PM cope 03_210 Mp_301 Allen Press x DTPro System File # 10TQ ROSENTHAL ET AL.ÐXIPHOPHORUS HYBRID ZONE 301 Fig. 2. Study sites and male morphometric trait distributions. Boxes and whiskers encompass 75% and 90% of trait variation respectively; horizontal line within box indicates median. Outside values and far outside values are indicated by asterisks and open circles, respectively. Lowercase letters indicate signi®cant differences in ANOVA for standard length and in ANCOVA for depth, dorsal ®n width, and sword extension length (see Materials and Methods). MC, Xiphophorus malinche, near Chicayotla; M, X. malinche,RõÂo Claro; HH, hybrid zone, Calnali-high; HM, hybrid zone, Calnali-mid; HL, hybrid zone, Calnali-low; HT, hybrid zone, TeocapaÂn; P, hybrid zone, A, Pochutla; B, Xiphophorus birchmanni. rus malinche were wild-caught or ®rst-generation test its departure from zero with a permutation descendants of collections in 1998±1999 from procedure. All statistical treatments and calcu- the type locality, the RõÂo Claro at Tlatzintla lations were performed using the randomiza- (208529510N, 988479560W), and X. birchmanni tion approach provided by the Genetix software were
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