Journal of Biogeography (J. Biogeogr.) (2012) ORIGINAL From the mountains to the sea: ARTICLE phylogeography and cryptic diversity within the mountain mullet, Agonostomus monticola (Teleostei: Mugilidae) Caleb D. McMahan1,2*, Matthew P. Davis3,OmarDomı´nguez-Domı´nguez4, Francisco J. Garcı´a-de-Leo´n5, Ignacio Doadrio6 and Kyle R. Piller1 1Department of Biological Sciences, ABSTRACT Southeastern Louisiana University, Aim The mountain mullet, Agonostomus monticola, is a diadromous fish wide- Hammond, LA, 70402, USA, 2LSU Museum spread throughout Middle America, occurring in rivers along the Atlantic and of Natural Science (Ichthyology), Department of Biological Sciences, Louisiana State Pacific slopes, as well as in the West Indies. Based on the disjunct distribution of University, Baton Rouge, LA, 70803, USA, this species, it has been hypothesized that this fish may represent more than one 3Department of Zoology, The Field Museum, taxon. The purpose of this study was to conduct a robust phylogeographical Chicago, IL, 60605, USA, 4Laboratorio de analysis of A. monticola across its range, using mitochondrial and nuclear mark- Biologı´a Acua´tica, Facultad de Biologı´a, ers. We aimed to investigate the potential for cryptic diversity and the time-scale Universidad Michoacana de San Nicola´sde of divergence in an effort to elucidate biogeographical episodes within Middle Hidalgo, Morelia, Michoaca´n, Me´xico, America in relation to the evolutionary history of Agonostomus monticola. 5Laboratorio de Gene´tica para la Location North and Middle America, including the West Indies. Conservacio´n, Centro de Investigaciones Biolo´gicas del noroeste (CIBNOR), S.C., La Methods Mitochondrial and nuclear sequence data (cyt b, S7-1) from individ- Paz, BCS, Me´xico, 6Departamento de uals throughout the range of the species were analysed phylogenetically using Biodiversidad y Biologı´a Evolutiva, Museo maximum-likelihood methodology. The oldest known fossil mullet was used as Nacional de Ciencias Naturales – CSIC, Jose a calibration to investigate divergence times for clades within A. monticola. Gutie´rrez Abascal 2, 28006, Madrid, Spain Results Results indicate four distinct lineages within the known range of A. monticola that largely correspond to oceanic basins (Caribbean, Gulf of Mexico, Pacific-A, Pacific-B). Divergence time estimates indicate early to mid- Miocene divergences for all four A. monticola clades, with Oligocene to Mio- cene divergences of internal nodes. Main conclusions These findings are congruent with geological hypotheses regarding movement of the Chortı´s block, as well as recent studies on the age *Correspondence: Caleb D. McMahan, Section of beginning emergence of the Panama Arc. of Ichthyology, LSU Museum of Natural Keywords Science, 119 Foster Hall, Baton Rouge, LA 70803, USA. Agonostomus monticola, diadromous, divergence times, fish, Middle America, E-mail: [email protected] mullet, North America, phylogeography. Middle America (e.g. gobies, sleepers and mullets). However, INTRODUCTION currently there are few studies that have investigated phylo- Middle America – the region comprising Mexico, Central geographical or population genetic patterns of a diadromous America and the Greater Antilles – hosts a diverse array of fish in this region (Cook et al., 2009). Given the nature of freshwater fishes that have been the focus of evolutionary their life history, diadromous species have the potential to and biogeographical studies (e.g. catfishes, Perdices et al., offer a different biogeographical perspective from that of pri- 2002; swamp eels, Perdices et al., 2005; tetras, Bermingham mary or secondary freshwater fishes. Processes that may have & Martin, 1998; Ornelas-Garcı´a et al., 2008; cichlids, Martin shaped the evolution of strictly freshwater or marine taxa & Bermingham, 1998; poeciliids, Rauchenberger, 1989). may have had different or no effects on diadromous taxa. Diadromous fishes, which utilize both freshwater and marine The mullet genus Agonostomus (Teleostei: Mugilidae) environments during their life cycle, occur throughout includes three species and is hypothesized to be sister to ª 2012 Blackwell Publishing Ltd http://wileyonlinelibrary.com/journal/jbi 1 doi:10.1111/jbi.12036 C. D. McMahan et al. most other mugilids (Harrison & Howes, 1991; Thomson, and Pacific lineages took place around 3–4 Ma (Lessios, 1997); recent work, however, suggests that Agonostomus is 2008), although some taxa show divergences prior to 4 Ma sister to the genus Mugil (Durand et al., 2012). The moun- (Murphy & Collier, 1996; Martin & Bermingham, 1998; tain mullet, Agonostomus monticola (Bancroft, 1834), was Hurt et al., 2009). In addition, recent geological evidence originally described from Jamaica and occurs in North, Cen- (1) shows that uplift of the Isthmus of Panama began in tral and South America along the Atlantic slope from North the late Oligocene (Farris et al., 2011), (2) suggests a nar- Carolina south to Venezuela (Berra, 2001) and along the rower seaway between Central and South America, and (3) Pacific slope from Baja California to Colombia (Miller et al., reconstructs the isthmus as an uninterrupted chain above 2005). The species also occurs throughout the West Indies sea level from the late Eocene to late Miocene (Montes (Greenfield & Thomerson, 1997). Most mainland records are et al., 2012). Depending on conditions, this could have led from Mexico and further south, although some records from to earlier divergences than previously hypothesized. Given the United States exist (summarized in Matamoros et al., the broad distribution of A. monticola, it is possible that 2009). The remaining two species, Agonostomus telfairii Ben- other geological features of Middle America may have nett, 1832 and Agonostomus catalai Pellegrin, 1932, occur played a role in shaping the phylogeographical patterns of sympatrically along the coast of Madagascar and Mauritius, this species. The Chortı´s block (Nuclear Middle America; with reports of each from surrounding areas (Thomson, encompassing El Salvador, Honduras, southern Guatemala 1997). Agonostomus has largely been neglected in systematic and part of Nicaragua) is one of the main geological struc- and biogeographical studies. tures in Middle America. Most models show the origin of Agonostomus monticola is typically found in tropical rivers the Chortı´s block in south-western Mexico, with a mid- with high flow (Matamoros et al., 2009), and the common Eocene eastward movement along the Motagua–Polochic name mountain mullet comes from the propensity of this fault, the current northern edge of the Chortı´s block (Rog- species to travel far upstream to elevations as high as ers et al., 2007; Hulsey & Lo´pez-Ferna´ndez, 2011). This 1500 m (Miller et al., 2005), although Loftus et al. (1984) structure has been shown to have played an important role reported collections from lentic bodies of water. In general, in the present-day distribution of Middle American fishes there is much to learn regarding the life history and ecology (Matamoros et al., 2012). of this species. While there is consensus that A. monticola is The objectives of this study are twofold: first, to conduct a diadromous species, there is substantial debate as to a robust phylogeographical investigation of A. monticola whether the species is catadromous (living in fresh water and across the range of this widespread species using both travelling to the ocean to spawn; Anderson, 1957; Cruz, mitochondrial and nuclear markers in an effort to identify 1987; Phillip, 1993) or amphidromous (with spawning events cryptic diversity and biogeographical patterns; and second, occurring in fresh water and juveniles subsequently carried to use this hypothesis of evolutionary relationships to inves- out to sea; Erdman, 1972; Pezold & Edwards, 1983). tigate the time-scale of divergence for lineages within Past morphological studies of A. monticola have led to A. monticola, to elucidate the timing of biogeographical contradictory findings that have resulted in 20 synonyms for events within Middle America in relation to the evolutionary the species (see Thomson, 1997, for a detailed taxonomic history of the species. Given the wide distribution of this history of this species). This is in part because many of species, the complex geological history of the region and the the characters previously used to diagnose populations of A. diversity of similarly distributed taxa, we hypothesize that monticola were found to be variable or associated with multiple evolutionary lineages will be recovered within this growth and development (e.g. thickness of the lip; Thomson, species. 1997). The family Mugilidae has been the focus of very few systematic studies (Schultz, 1946; Harrison & Howes, 1991; MATERIALS AND METHODS Thomson, 1997; Durand et al., 2012), and there are no pre- vious works that specifically investigated the intraspecific Specimen collection and taxon sampling geographical variation of A. monticola. Given the allopatric distribution of this species (Pacific/Atlantic), some authors Samples of A. monticola were acquired from throughout the have suggested that A. monticola may include cryptic species range of the species (see Appendix S1 in Supporting Infor- diversity (Harrison, 2002; Miller et al., 2005). Studies of sim- mation). Most specimens were collected with seines and ilarly distributed aquatic species (shrimp, Hurt et al., 2009; backpack electrofishers from freshwater rivers across Mexico, fish, Grant & Leslie, 2001; Tringali et al., 1999; for a sum- Cuba,