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Assessing Population-Level Morphometric Variation of the Mountain Mullet Agonostomus Monticola (Teleostei: Mugilidae) Across Its Middle American Distribution

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Assessing Population-Level Morphometric Variation of the Mountain Mullet Agonostomus Monticola (Teleostei: Mugilidae) Across Its Middle American Distribution Neotropical Ichthyology, 15(4): e170036, 2017 Journal homepage: www.scielo.br/ni DOI: 10.1590/1982-0224-20170036 Published online: 21 December 2017 (ISSN 1982-0224) Copyright © 2017 Sociedade Brasileira de Ictiologia Printed: 18 December 2017 (ISSN 1679-6225) Assessing population-level morphometric variation of the Mountain Mullet Agonostomus monticola (Teleostei: Mugilidae) across its Middle American distribution Bertha P. Díaz-Murillo1, Gorgonio Ruiz-Campos2, Kyle R. Piller3, Caleb D. McMahan4, Francisco J. García-De-León5 and Faustino Camarena-Rosales1 Population-level morphometric variation of the Mountain Mullet (Agonostomus monticola) was assessed in 419 adult specimens from 25 sample sites (river basins) across its Middle American distribution (Pacific and Atlantic-Caribbean drainages). This analysis was based on 36 standardized linear measurements and 19 landmarks on geometric morphometrics approach. Discriminant function analysis (DFA) revealed 19 linear morphological characters with significant variation among groups. Geometrically, the most notable changes were associated to the curvature of the frontal region of the head, the anterior and posterior insertion of the first dorsal and anal fins. The resulting grouping based on the DFA and geometric morphometrics techniques (Pacific-A, Pacific-B and NE México-Caribbean) were similar to those previously recovered by genetic techniques, where the Pacific-B (Ayuquila river basin) was the most different group. Our results provide morphological evidence for considering Agonostomus monticola as a complex of evolutionary entities, represented by two forms in the Pacific Ocean and another in the Atlantic Ocean. Keywords: Discriminant analysis, Evolutionary entities, Landmarks, Middle American distribution, Morphometry. La variación morfométrica de poblaciones de la lisa de montaña Agonostomus monticola fue evaluada en 419 especímenes adultos recolectados en 25 sitios (cuencas) a través de su distribución mesoamericana (Pacífico, Atlántico y cuencas del Caribe). El análisis fue basado en 36 medidas lineales estandarizadas y 19 puntos de referencia basados en morfometría geométrica. El análisis de función discriminante (AFD) reveló 19 caracteres morfométricos con variación significativa entre grupos. Geométricamente, los cambios más notables estuvieron asociados con la curvatura de la región frontal de la cabeza y la inserción anterior y posterior de la primera aleta dorsal y de la aleta anal. Los agrupamientos resultantes del AFD y del análisis de morfometría geométrica (Pacífico-A, Pacífico-B y NE México-Caribe) fueron similares con los previamente definidos mediante técnicas genéticas. El grupo Pacífico-B (cuenca de Ayuquila) fue el más disímil. Nuestros resultados proveen evidencia morfológica para considerar a Agonostomus monticola como un complejo de entidades evolutivas, representadas por dos formas en la cuenca del océano Pacífico y una forma en la cuenca del océanoAtlántico. Palabras clave:Análisis discriminante, Distribución mesoamericana, Entidades evolutivas, Morfometría, Puntos de referencia. Introduction are diadromous and move between freshwater and marine waters (Harrison, Howes, 1991). Taxonomic nomenclature The family Mugilidae, commonly known as “mullets,” among members of this family has been a common theme includes 75 currently recognized species (Nelson, 2006; of discussion (cf. Ghasemzadeh, González-Castro, 2016), Froese, Pauly, 2016). Most are largely marine and inhabit where at least 280 nominal species have been described of mainly estuarine-lagoon environments of tropical and which only 75 are currently recognized as valid (Harrison et subtropical regions of the world (Thomson, 1997; Castro- al., 2007; Durand et al., 2012). The few revisionary studies Aguirre et al., 1999); however, a few species in the family of the family Mugilidae (e.g., Harrison, Howes, 1991; 1Facultad de Ciencias Marinas, Universidad Autónoma de Baja California, Ensenada, Baja California 22800, México. (BPDM) diazp_2000@ yahoo.com, (FCR) [email protected] 2Facultad de Ciencias, Universidad Autónoma de Baja California, Ensenada 22800, México. US mailing address: PMB 064, P.O. Box 189003, Coronado CA 92178-9003. Phone: +(52) 646 121 0330. [email protected] (corresponding author) 3Southeastern Louisiana University, Department of Biological Sciences, Hammond, LA 70402, USA. [email protected] 4The Field Museum of Natural History, 1400 S. Lake Shore Drive, Chicago, IL 60605, USA. [email protected] 5Laboratorio de Genética para la Conservación. Centro de Investigaciones Biológicas del Noroeste. La Paz, Baja California Sur 23096, México. [email protected] e170036[1] Neotropical Ichthyology, 15(4): e170036, 2017 2 Morphological variation of the Agonostomus monticola Thomson, 1997) have fallen into frequent contradictions Material and Methods on the taxonomy of its members, in part because of the conservative morphology (Aurelle et al., 2008) and limited Voucher specimens of A. monticola examined in this number of specimens examined along the distributional study were came from 25 localities throughout Middle range of each species. However, the recent application America including coastal states from the Mexican Pacific of new techniques and procedures (molecular taxonomy (Sinaloa to Chiapas, including Baja California Sur; referred and geometric morphometrics) in the study of the family to as Pacific-A), from the Atlantic of northeastern México Mugilidae have provided a different perspective on (Tamaulipas and San Luis Potosí; referred to as NE México) phylogeny of the taxa in this group, including the presence and from the Caribbean region of Honduras to Panama of cryptic species (Durand, Borsa, 2015; Ghasemzadeh, including Jamaica (Fig. 1). Additionally, we referred specimens González-Castro, 2016). from Ayuquila drainages in Jalisco, México as Pacific-B Despite the commercial value, abundance and wide following McMahan et al. (2013). All specimens examined in distribution of mullets, some species are taxonomically this study are from fish collections of the Centro Universitario (Phillip, 1993; Aurrelle et al., 2008; Durand et al., 2012) and de Ciencias Biológicas y Agropecuarias (CUCBA-UDG) in biologically (Froese, Pauly, 2016) poorly known. One such Guadalajara, Jalisco, México; The Field Museum of Natural group is the genus Agonostomus, which includes A. monticola History (FMNH), in Chicago, Illinois, USA; Louisiana State (Bancroft, 1834), A. telfairii Bennett, 1832 and A. catalai University Museum of Natural Science (LSUMZ) in Baton Pellegrin, 1932 (cf. Harrison, Howes, 1991; Thomson, 1997; Rouge, Louisiana, USA; Southeastern Louisiana University McMahan et al., 2013). Within the genus, A. monticola is (SLU) in Hammond, Louisiana, USA; Universidad Autónoma the most widespread species, occurring along both sides de Baja California (UABC) in Ensenada, Baja California, of the American continent from the Yaqui river in Sonora, México; Universidad Autónoma de Nuevo León (UANL) México (Hendrickson et al., 1980) including drainages in in Monterrey, Nuevo León, México; University of Southern Baja California Sur (Follett, 1960; Ruiz-Campos et al., Mississippi (USM) in Hattiesburg, Mississippi, USA. A list of 2002) to Colombia; on the Atlantic slope, it is distributed fish material examined appears in Appendix (S1 - Available from Florida (USA) (Contreras-Balderas, 1972; García-De- only as online supplementary file accessed with the online León et al., 2005) to Venezuela as well as the islands of the version of the article at http://www.scielo.br/ni). West Indies (Castro-Aguirre et al., 1999; Miller, 2005). This species prefers lotic habitats with waterfalls, from the coast to 650 m above sea level, in a temperature range from 21 to 29°C (Cotta-Ribeiro, Molina-Ureña, 2009). Recently, molecular studies of A. monticola have indicated that the species may be more diverse than currently recognized. In this sense, Durand et al. (2012) conducted a family-wide phylogenetic study of Mugilidae using multiple mitochondrial markers. They recovered a non-monophyletic Agonostomus, and demonstrated the existence of multiple lineages within the widespread A. monticola. Later, McMahan et al. (2013) conducted a phylogeographic study of A. monticola based also on molecular data (mitochondrial and nuclear) and recovered four lineages, with origins from the late to middle Miocene (14.7 to 7.0 million years). Despite the fact that A. monticola has been traditionally Fig. 1. Map showing specimen localities for Agonostomus considered as one morphotype in America (Nelson, 2006), monticola. Pacific- A: blue circles (1= La Paz, 2= El Fuerte, the widespread distribution coupled with the results from 3=Sinaloa, 4= San Lorenzo, 5= Piaxtla, 6= Presidio, 7= molecular phylogenetic studies suggests that this species is Baluarte, 8= Ameca, 9 = Los Arcos, 10= Pitillal, 11= María in need of morphological study, as multiple lineages may García, 13=Purificación, 14= Verde, and 15= Suchiate), be present. No previous study for evaluating morphological Pacific-B: pink circle (12= Ayuquila), NE México: green variation throughout the distributional range of this circles (16 = Matamoros, 17= San Luis Potosí), and species is known (Castro-Aguirre et al., 1999); therefore, Caribbean: purple circles (18= Milk River, 19= Lancetilla, this is the first assessment to characterize and quantify 20 = Danto, 21= Cuero and Salado, 22= Bonito, 23= Limón, the morphological variation of A. monticola in its Middle 24= Boca del Toro,
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