Molecular phylogeny and biogeography of the Cuban genus Girardinus Poey, 1854 and relationships within the tribe Girardinini (Actinopterygii, Poeciliidae)
Introduction
The tribe Girardinini Hubbs, 1924 was proposed to comprise 6 genera and 15 species and subspecies of endemic freshwater fishes from the main island of Cuba and Juventud island (former Pinos) (Rivas, 1958, Barus et al., 1991). However, according to the taxonomy of Rosen and Bailey (1963), the tribe is only considered to have three genera (Girardinus Poey, 1854; Quintana Hubbs, 1934 and Carlhubbsia Withley, 1951) and a number of species (from ten to twelve) that depends on the describing author (Rosen and Bailey, 1963, Parenti and Rauchenberger, 1989, Ghedotii, 2000, Lucinda and Reis, 2005). The monotypic genus Quintana is represented by the species Quintana atrizona Hubbs, 1934 inhabiting both Juventud Island and western Cuba Island. The genus Carlhubbsia has two recognized species: C. kidderi (Hubbs, 1936) from Mexico and Guatemala, and C. stuarti Rosen and Bailey, 1959 from Guatemala and Belize. In turn, the genus Girardinus has eight recognized species (Lucinda, 2003): G. metallicus Poey, 1854; G. uninotatus Poey, 1860; G. creolus Garman, 1895; G. denticulatus Garman, 1895; G. cubensis (Eigenmann, 1903); G. falcatus (Eigenmann, 1903); G. microdactylus Rivas, 1944 and G. rivasi Barus and Wohlgemuth, 1994.
The genus Girardinus is among the endemic freshwater fishes that inhabit both the islands of Cuba and Juventud. This genus shows its highest diversity in western Cuba and is absent from central Cuba south of the Sancti-Spiritus district and from some eastern areas of Cuba Island, such as short rivers south of the Sierra Maestra and west of Sagua-Baracoa. Compared to other freshwater fishes of the Antillean islands, Girardinus is a good model for deciphering the evolutionary history of Cuban hydrographical systems because of its wider range of distribution throughout Cuba, its higher diversity, its presence on two islands of known geological age and its ecology, being more restricted to freshwater systems. Studies on the salt tolerance of representatives of Girardinini have failed to recover fishes from salt, brackish, or fresh water with a Cl− content higher than 1000 parts per million (Rivas, 1958, Rivas, 1986). We can therefore assume that dispersion in Girardinini occurs only via connected freshwater systems (Rivas, 1958).
Models of the palaeogeography of Cuba based on biological data can be useful for geological reconstructions, since Cuba occupies one of the most geologically complex areas of the planet. Cuba’s main and Juventud islands boast over 600 fluvial systems mostly crossing karst landscapes. The country’s karst topography determines that some rivers are fragmented by waterfalls or disappear for kilometers underground and may also be the cause of local speciation events in freshwater fishes such as Girardinus with a limited capacity for dispersal. By identifying the barriers that caused the fragmentation and dispersion of freshwater fishes and the timing of these events in a geological scenario, insight can be gained into the evolution of organisms and areas. Effectively, studies on the biogeography of freshwater fishes in Central America and the Caribbean Islands have contributed significantly to palaeobiogeography models (Rosen, 1975, Rosen, 1978, Rosen, 1985, Nelson and Rosen, 1981).
The genus Girardinus has also been examined as a means of biologically controlling disease-transmitting mosquitoes (Rodríguez et al., 2004, Menéndez Díaz et al., 2007); other studies have focussed on its complex taxonomy (Barus et al., 1981, Barus et al., 1986, Barus et al., 1991, Barus et al., 1998, Barus and Libosvarsky, 1986, Barus and Wohlgemuth, 1994). Most of the latter works have focused on basic aspects such as taxonomy, geographical distribution and ecological requirements. In contrast, there are only a few models of the phylogenetic relationships and biogeography of this genus. The first and most developed model is that proposed by Rivas (1958), in which the ancestor of today’s Girardinus colonized Cuba from the eastern Yucatan during the Upper Miocene–Pliocene across an intercontinental Yucatan-Cuba landbridge. Western Cuba is considered the center of origin of Girardinus, where it shows its highest diversity, and its speciation is thought to have occurred during the Pleistocene. The ancestral species of the genus is considered by Rivas (1958) to be similar to Girardinus creolus, which is the only species confined to upper stream reaches (Fig. 1). Rodriguez et al. (1992) corroborated the model suggested by Rivas (1958) considering Girardinus creolus to be the ancestral species of the genus Girardinus. An eastern Yucatan-Cuba connection was also supported by the phylogenetic relationships proposed by Rosen and Bailey (1963), who considered the genera Quintana from Cuba and Carlhubbsia from eastern Yucatan and Guatemala, as sister genera of Girardinus.
However, recent studies on poeciliid fishes question the Yucatan-Cuba connection as well as the relationship of Carlhubbsia as sister group of the genera Girardinus and Quintana (Hrbek et al., 2007). An alternative model has been developed to explain the presence of Poeciliidae representatives in the Antilles, including the tribe Girardinini across GAARlandia (Greater Antilles + Aves Ridge) (Iturralde-Vinent and MacPhee, 1999, Iturralde-Vinent, 2006). This model of geological evolution of the Caribbean basin suggests that the Greater Antilles did not permanently emerge until the Eocene-Oligocene boundary (30–35 mya), when they were connected to northern South America by the Aves Ridge. The three biogeographical models (Rivas, 1958, Rosen and Bailey, 1963, Hrbek et al., 2007) are represented in Fig. 2.
The present study was designed to test previous phylogenetic relationships of the tribe Girardinini (Rivas, 1958, Rosen and Bailey, 1963) and the three biogeographical models proposed for the Cuba and Juventud islands (Fig. 2) using the most complete molecular dataset for the tribe Girardinini available to date.
Section snippets
Sampling
DNA samples were analyzed in 111 individuals representing all described species of the genus Girardinus (except G. cubensis). Populations were collected in the wild from 48 localities of the Cuba and Juventud islands including the type locality when possible (Table 1); (Fig. 3). DNA was extracted from the dorsal muscle, which was preserved in liquid nitrogen or 70% ethanol. Voucher specimens of these species were deposited in the collections of the Tropical Medicine Institute Pedro Kouri, La
Phylogenetic analysis
The mitochondrial (cytochrome b) and two nuclear (RAG-1 and β-actin) genes sequenced rendered 3590 characters (1140 mitochondrial and 2450 nuclear). Base frequencies were homogeneous across all sites (cytochrome b: χ2 = 122.22, df = 384, p = 1.0; RAG-1: χ2 = 16.68, df = 72, p = 1.0, β-actin: χ2 = 4.30, df = 72, p = 1.0). For cytochrome b, 665 sites were variable and 538 were parsimony informative (47.2%). According to codon position, the most informative was the third (335 parsimony informative characters),
Phylogeny of Girardinini and taxonomical implications
Our data resulted in a well-resolved phylogeny for the tribe Girardinini, although relationships between Girardinini and other poeciliids could not be resolved using our mitochondrial and nuclear gene data. Our analyses did not support the monophyly of the tribe Girardinini as proposed by most authors (Rosen and Bailey, 1963, Parenti and Rauchenberger, 1989, Ghedotii, 2000, Lucinda and Reis, 2005). Also contrary to the findings of previous morphological studies (Rosen and Bailey, 1963,
Acknowledgments
We are grateful to R. Fimia Duarte, M. Díaz Pérez, A. Chamizo, V. Rivalta, A. de Sostoa, P. Garzon and O. Dominguez for help in field collection. D. McAllister and K. de Jong sent us valuables specimens. A. Burton reviewed the English of the manuscript. We also thank L. Rojas Rivero for her support and M. Iturralde-Vinent for helpful suggestions while preparing the manuscript. This study was financed by project A/9998/07.
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