The Evolutionary History of the Goby Elacatinus Puncticulatus in the Tropical Eastern Pacific: Effects of Habitat Discontinuities and Local Environmental T Variability
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Molecular Phylogenetics and Evolution 130 (2019) 269–285 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev The evolutionary history of the goby Elacatinus puncticulatus in the tropical eastern pacific: Effects of habitat discontinuities and local environmental T variability E.R. Sandoval-Huertaa,b, R.G. Beltrán-Lópezc,d, C.R. Pedraza-Marróna,b, M.A. Paz-Velásqueze, ⁎ A. Angulof, D.R. Robertsong, E. Espinozah, O. Domínguez-Domínguezb, a Programa Institucional de Maestría en Ciencias Biológicas, Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo, Edificio “R” planta baja, Ciudad Universitaria, Morelia, Michoacán 58030, Mexico b Laboratorio de Biología Acuática, Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo, Edificio “R” planta baja, Ciudad Universitaria, Morelia, Michoacán 58030, Mexico c Programa Institucional de Doctorado en Ciencias Biológicas, Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo, Edificio “R” planta baja, Ciudad Universitaria, Morelia, Michoacán 58030, Mexico d Laboratorio de Ictiología, Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Morelos, Av. Universidad no. 1001, Cuernavaca, Morelos 62209, Mexico e Centro de Estudios del Mar y Acuicultura, Universidad de San Carlos de Guatemala, Guatemala City, Guatemala f Museo de Zoología y Centro de Investigación en Ciencias del Mar y Limnología, Universidad de Costa Rica. 11501–2060, San Pedro de Montes de Oca, San José, Costa Rica g Naos Marine Laboratory, Smithsonian Tropical Research Institute, Balboa, Panama h Dirección del Parque Nacional Galápagos, Puerto Ayora, Islas Galápagos, Ecuador ARTICLE INFO ABSTRACT Keywords: Habitat discontinuities, temperature gradients, upwelling systems, and ocean currents, gyres and fronts, can Biogeographic barriers affect distributions of species with narrow environmental tolerance or motility and influence the dispersal of Habitat discontinuities pelagic larvae, with effects ranging from the isolation of adjacent populations to connections between them. The Mesoscale eddies coast of the Tropical Eastern Pacific (TEP) is a highly dynamic environment, with various large gyres and Upwellings upwelling systems, alternating currents and large rocky-habitat discontinuities, which may greatly influence the Reef-fishes genetic connectivity of populations in different parts of the coast. Elacatinus puncticulatus is a cryptic, shallow- Tropical Eastern Pacific living goby that is distributed along the continental shore of virtually the entire TEP, which makes it a good model for testing the influence of these environmental characteristics in the molecular evolution of widespread species in this region. A multilocus phylogeny was used to evaluate the influence of habitat gaps, and ocea- nographic processes in the evolutionary history of E. puncticulatus throughout its geographical range in the TEP. Two well-supported allopatric clades (one with two allopatric subclades) were recovered, the geographic dis- tribution of which does not correspond to any previously proposed major biogeographic provinces. These po- pulations show strong genetic structure and substantial genetic distances between clades and sub-clades (cytb 0.8–7.3%), with divergence times between them ranging from 0.53 to 4.88 Mya, and recent population ex- pansions dated at 170–130 Kya. The ancestral area of all populations appears to be the Gulf of Panama, while several isolation events have formed the phylogeographic patterns evident in this species. Local and regional oceanographic processes as well as habitat discontinuities have shaped the distribution patterns of the genetic lineages along the continental TEP. Large genetic distances, high genetic differentiation, and the results of species-tree and phylogenetic analyses indicate that E. puncticulatus comprises a complex of three allopatric species with an unusual geographic arrangement. ⁎ Corresponding author. E-mail addresses: [email protected] (R.G. Beltrán-López), [email protected] (D.R. Robertson), [email protected] (E. Espinoza), [email protected] (O. Domínguez-Domínguez). https://doi.org/10.1016/j.ympev.2018.10.020 Received 10 May 2018; Received in revised form 5 September 2018; Accepted 15 October 2018 Available online 23 October 2018 1055-7903/ © 2018 Elsevier Inc. All rights reserved. E.R. Sandoval-Huerta et al. Molecular Phylogenetics and Evolution 130 (2019) 269–285 1. Introduction they occur and on the region as a whole (Fiedler, 2002; Pennington et al., 2006; Fernández-Álamo and Färber-Lorda, 2006). Genetic connectivity among populations of marine organisms is The red-head goby, Elacatinus puncticulatus (Ginsburg, 1938), the strongly determined by the dispersal capability of the species and by only member of this neotropical genus in the eastern Pacific, is wide- barriers that may prevent or limit dispesal (Pineda et al., 2007; Cowen spread along the mainland of TEP, ranging from the central Gulf of and Sponaugle, 2009). For marine organisms some barriers are im- California to southern Ecuador. Malpelo Island, a tiny rock offshore passible and completely obstruct marine corridors, e.g. land masses from Colombia, is the only oceanic island in the TEP at which E. such as the Central American isthmus (Lessios, 2008); while others are puncticulatus has been recorded (Robertson and Allen, 2015), although permeable, and even large stretches of open ocean can be crossed by that likely is as a vagrant, as that record is new and it was not seen at some species (e. g. the Eastern Pacific Barrier; Robertson et al., 2004; Malpelo by divers searching for it there in 2018 (A. Polanco, pers. com. Lessios and Robertson, 2006). to DRR). Adults of E. puncticulatus live on rocky reefs, frequently in Large habitat discontinuities are considered to be one of the main association with sea urchins in shallow water (< 21 m) (Patzner et al., barriers to dispersal and expansion of the geographic ranges of reef- 2011; Robertson and Allen, 2015). Elacatinus species produce benthic fishes (Riginos and Nachman, 2001), by eliminating available suitable eggs, from which pelagic larvae hatch (Colin, 1975). The pelagic larval habitat for establishment at the end of the larval stage. In the Tropical stage of three Caribbean species of Elacatinus ranges from means of Eastern Pacific (TEP) two large stretches of sandy and muddy shoreline 21–38 days (Luiz et al., 2013; Rickborn and Buston, 2015). The larval represent such barriers for shallow-water reef fishes that have been duration of E. puncticulatus is not known. proposed as the limits of biogeographic provinces in the mainland TEP: The adult and likely larval characteristics of E. puncticulatus, to- the ∼525 km long Central American Gap between southern Mexico and gether with its widespread distribution in a range of subtropical and El Salvador, and the 370 km wide Sinaloan Gap on the southeast shore tropical environments across 34 degrees of latitude and > 5000 km of of the Gulf of California. (Ekman, 1953; Springer, 1959; Walker, 1960; the continental shore of virtually the entire TEP, make this species a Briggs, 1974; Hastings, 2000; Robertson and Cramer, 2009; Briggs and good model subject for testing how large habitat discontinuities and Bowen, 2012). Three biogeographic provinces relating to effects of oceanographic process may have affected genetic connectivity and these two gaps have been defined by the differences in species richness variation across populations, and whether the distribution of genetic and levels of endemism (see Fig. 1A). If effects of these sandy gaps as lineages parallels that of major recognized biogeographic subunits of barriers have produced such differences then their restrictive effects on the TEP. To do so we used mitochondrial and nuclear markers from the distributions of species should also be reflected in a genetic differ- individuals collected at sites between the northern and southern limits entiation between populations of the same species in different pro- of its continental range, in all three generally recognized continental vinces (Muss et al., 2001). However, in various reef fishes that are biogeographic provinces, to examine genetic relationships between widely distributed along the continental shore of the TEP, no evidence populations at different locations and provinces. of phylogeographic patterns related to the location of the two sandy gaps or the biogeographic provinces have been reported. These include 2. Materials and methods the blenniid Ophioblennius steindachneri (Muss et al., 2001); the serranid Epinephelus labriformis (Craig et al., 2006), four species of the haemulid 2.1. Specimen collection genus Anisotremus (Bernardi et al., 2008); the pomacanthid Holacanthus passer, and the pomacentrid Abudefduf troschelii (Bernardi et al., 2014). A total of 202 individuals of E. puncticulatus were collected in 39 Lessios and Baums (2017) provide examples of various invertebrate localities throughout the continental range of the species (Fig. 1B, taxa and circumtropical reef-fishes that lack of geographic genetic Table 1). The specimens were collected while SCUBA diving, using an structure related to those two barriers. In such cases, larval dispersal anesthetic solution of 5% clove oil in ethanol. Tissue samples comprised capability and biological and ecological traits evidently are more im- a pectoral fin of each individual, preserved in 95% ethanol and, stored portant than barriers produced by