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Molecular Phylogeny of the Live-Bearing Fish Genus Poecilia (Cyprinodontiformes: Poeciliidae) Felix Breden,* Margaret B

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Molecular Phylogeny of the Live-Bearing Fish Genus Poecilia (Cyprinodontiformes: Poeciliidae) Felix Breden,* Margaret B Molecular Phylogenetics and Evolution Vol. 12, No. 2, July, pp. 95–104, 1999 Article ID mpev.1998.0600, available online at http://www.idealibrary.com on Molecular Phylogeny of the Live-Bearing Fish Genus Poecilia (Cyprinodontiformes: Poeciliidae) Felix Breden,* Margaret B. Ptacek,† Michael Rashed,* Donald Taphorn,‡ and Carlos Augusto Figueiredo§ *Behavioural Ecology Research Group and Institute of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, British Columbia, Canada V5A 1S6; †Department of Biological Sciences, Idaho State University, Pocatello, Idaho 83209-8007; ‡Museo de Ciencias Naturales, UNELLEZ, Guanare, Edo. Portuguesa, Venezuela 3310; and §Departamento de Zoologia, Laborato´ rio de Ictiologia Geral e Aplicada, Universidade Federal do Rio de Janeiro, Rio de Janeiro, CEP 21944-970 Brazil Received December 2, 1997; revised September 14, 1998 United States to Bolivia and southern Brazil. Species of Members of the genus Poecilia exhibit extensive Poecilia are found in a wide range of habitats, exhibit morphological, behavioral, and life history variation morphological and behavioral differentiation within within and between species. This natural variation, and between species, and have been studied exten- coupled with short generation times and the ease with sively for the effects of natural and sexual selection. We which members of this genus can be cultured in the present a phylogeny of this genus based on NADH lab, have made several species model systems for Dehydrogenase Subunit 2 (ND2) sequence variation, in studying the effects of sexual and natural selection on order to resolve some of the relationships within Poe- the evolution of natural populations. Given that there cilia and to provide a phylogenetic context for studies of is no clear understanding of the phylogenetic relation- ships within the genus, these studies have not been put sexual selection in this group. into a historical context, and between-species compari- sons have been limited. We sequenced the complete Taxonomy NADH Dehydrogenase Subunit 2 (ND2) mitochondrial The following description of four subgenera follows gene (1047 bp) in representatives of the major divi- Rosen and Bailey (1963), with notes from Rauchenberg- sions of the genus in order to examine these relation- er’s (1989) annotated list of species in the subfamily ships. The subgeneric groups of Rosen and Bailey Poeciliinae. Table 1 outlines these major divisions (1963) are, for the most part, supported, with some within the genus and the specimens examined in this adjustment within the subgenera Poecilia and Pam- study. We also review proposed taxonomies that have phorichthys. The morphological distinctness of the reinstated or adopted the genus rank for some of the groups within Poecilia suggest that the original ge- assemblages within Poecilia (e.g., Costa, 1991; Meyer, neric designations be reinstated, but this awaits a 1993; Rodriquez, 1997). more thorough analysis. Two implications from the Subgenus Poecilia includes at least 20 named species phylogeny are particularly relevant to sexual selection studies: within the North and Central American mol- from North and Central America and northeastern lies, the three species of sailfin mollies form a monophy- South America that are commonly referred to as mol- letic group, and within the subgenus Lebistes, the lies. This subgenus includes the previously named sister taxon to the guppy, P. reticulata, is most likely genera, Mollienesia LeSueur, 1821 and Allopoecilia the group of species previously designated as Hubbs, 1924. The North and Central American mollies Micropoecilia. ௠ 1999 Academic Press (referred to as group Mollienesia within the subgenus Poecilia by Rauchenberger (1989)) have been divided into two species complexes: P. latipinna and P. sphenops INTRODUCTION (Hubbs, 1933; Miller, 1983). The P. latipinna complex, or ‘‘sailfin’’ mollies, includes three species, P. latipinna, As part of their revision of the family Poeciliidae, P. petenensis, and P. velifera, and males of all three Rosen and Bailey (1963) placed several well-estab- species are sexually dimorphic, having an enlarged lished genera, including Mollienesia, Allopoecilia, dorsal fin used in a courtship display directed toward Limia, Pamphorichthys, Lebistes, and Micropoecilia, females (Ptacek and Travis, 1997). These three species into one genus, Poecilia, retaining four subgenera. The are confined to the Atlantic slope and range from the resulting genus, Poecilia, is a complicated and widely southern United States southeastward into northern distributed group, ranging from the southeastern Guatemala and northern Belize. Possession of the 95 1055-7903/99 $30.00 Copyright ௠ 1999 by Academic Press All rights of reproduction in any form reserved. 96 BREDEN ET AL. ‘‘sailfin’’ distinguishes these species from the remaining Bailey, 1963), but these do not include species placed in ‘‘shortfin’’ molly species in the P. sphenops complex. The Odontolimia (Rivas, 1980) (Table 1). P. sphenops complex was originally thought to include a Rodriquez (1997) provides the most recent revision of single, variable, and widespread species, but more the genus Poecilia (sensu Rosen and Bailey, 1963) recently Quesada (1971) suggested dividing it into two based on a cladistic analysis of 27 morphological charac- species complexes: P. sphenops and P. mexicana. The P. ters. His analysis follows Costa (1991) by recognizing mexicana complex contains eight described species the genus Pamphorichthys and Rivas (1980) by recogniz- found on the Atlantic slope of Mexico and into Central ing the genus Limia, while retaining species from the America to Nicaragua. The P. sphenops complex con- subgenera Lebistes and Poecilia in a genus that he tains four described species from the Pacific slope of recognized as Poecilia. Mexico. The gynogenetic unisexual Amazon molly, P. formosa, is included in the P. mexicana species complex, Sexual Selection Studies but is a known hybrid between one member of the A number of species in the genus Poecilia exhibit sailfin complex, P. latipinna, and one shortfin species, highly colorful males, elaborate courtship, and sexual P. mexicana (Avise et al., 1991; Schartl et al., 1995). We dimorphism associated with sexual selection (reviewed examined six species of the Mollienesia group, includ- in Farr, 1989). Two groups in particular, sailfin mollies ing three shortfin species and all three sailfin species, and the guppy, have become model systems for the and one species outside of Mollienesia, P. vivipara, to study of sexual selection. Evaluating the role of sexual test for monophyly of the sailfin mollies and to examine selection in the differentiation and speciation of these the relationship of P. vivipara to the Mollienesia group groups will be possible only in the context of a resolved (Table 1). phylogeny. Subgenus Lebistes consists of the guppy, P. reticulata, In the subgenus Poecilia, female preference for mor- three species previously placed in the genus Micropoe- phological and behavioral features associated with the cilia (P. parae, P. picta, and P. branneri), and a fifth sailfin phenotype has been demonstrated for the sailfin species, P. amazonica, closely allied to P. parae. Re- species P. latipinna (Ptacek and Travis, 1997). Since cently, Meyer (1993) redescribed Micropoecilia bifurca the same morphological and behavioral traits that and reinstated the genus Micropoecilia. The guppy has differ among conspecific populations also distinguish been studied extensively for variation in life history, sailfin species from shortfin species (Ptacek, 1998), it is behavior, and morphology as a response to variation in likely that sexual selection played an important role in habitat and sexual selection. In our study we examined speciation of sailfin mollies as well. One of our goals is two P. reticulata specimens, one from the Oropuche to resolve whether or not the sailfin molly species are drainage (Oro) and one from the Caroni drainage (Car) the result of a single speciation event and subsequent in Trinidad. These are two genetically distinct groups diversification, leading to the three extant species, or (Carvalho et al., 1991; Fajen and Breden, 1992). We are the result of multiple independent origins of the also included one specimen of P. picta and one of P. sailfin phenotype. parae (Table 1). The subgenus Lebistes is considered to exhibit the Subgenus Pamphorichthys, as described by Rosen greatest degree of sexual dichromatism and male poly- and Bailey (1963), consists of P. minor from the Amazon morphism in the family Poeciliidae (Rosen and Bailey, drainage, P. hollandi from Rio Sao Francisco drainage 1963; Farr, 1989). The amount of male coloration and and south, P. hasemani, poorly described and listed courtship activity varies dramatically among popula- from the Rio Paraguay drainage in Bolivia, and P. tions of the guppy, P. reticulata, depending in part on heterandria from a restricted coastal area of Venezuela. level of predation (Houde, 1997). There is also a wide Costa (1991) confirmed P. hasemani from several locali- range of male coloration patterns exhibited among the ties in Brazil, included Cnesterodon scalpridens from species previously described as Micropoecilia. P. picta is the Amazon basin in the genus (thought to be in the strongly dichromatic, but males are essentially mono- subgenus Lebistes by Rosen and Bailey (1963)), and morphic throughout the geographic range (Breden et described a sixth species, Pamphorichthys araguaien- al., unpublished
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