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(Perciformes, Pomacentridae) in the Eastern Pacific

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(Perciformes, Pomacentridae) in the Eastern Pacific Mar Biol (2015) 162:2291–2303 DOI 10.1007/s00227-015-2759-9 ORIGINAL PAPER Adaptive radiation of damselfishes (Perciformes, Pomacentridae) in the eastern Pacific Rosalía Aguilar‑Medrano1,2 · Héctor Reyes‑Bonilla3 · P. David Polly4 Received: 8 July 2015 / Accepted: 5 October 2015 / Published online: 23 October 2015 © Springer-Verlag Berlin Heidelberg 2015 Abstract Pomacentridae is one of the most abundant damselfishes: in islands, the distance of the island to the families in tropical and temperate rocky and coral reefs. mainland and the size of the island; while in the mainland, They present an extraordinary diversity of habitat prefer- the temperature appears to be the main barrier. Our results ences, feeding, morphologies and behavior. The eastern show the radiation process of Pomacentridae in the eastern Pacific is biogeographically isolated by the Isthmus of Pacific as a dynamic dispersion system, which can be cat- Panama and the eastern Pacific barrier. There is an agree- egorized in three main steps: (1) mixture and speciation of ment about the origin of the fauna of the Tropical Eastern species with close affinity to west Atlantic ancestral stocks Pacific, suggesting three main factors, mixture, disper- in the Central Province, (2) dispersion due to favorable sal and vicariance. In this study, by cluster analyses and conditions to Galapagos islands and Gulf of California and parsimony analysis of endemism, the distribution of dam- (3) the more complex and perhaps long, gradual dispersal selfishes within the eastern Pacific was analyzed to elu- and radiation to temperate areas and isolated or marginal cidate the provinciality and the history of their radiation. environments. Six main provinces were found: (1) Easter Pacific equato- rial islands, (2) North, (3) Center, (4) South, (5) Califor- nia Province and (6) Clipperton. The Gulf of California Introduction and Galapagos islands are the two main centers of spe- cies richness. Three main factors limited the radiation of While the earliest divergences among perciform fishes may have occurred in the rudist-dominated Cretaceous car- bonate platforms during the fragmentation of Gondwana Responsible Editor: M. Taylor. (about 75 My) (Kauffman and Fagerstrom 1993; Bellwood et al. 2004), the radiation of the Pomacentridae and other Reviewed by X. Moreno and an undisclosed expert. reef fish families was closely associated with the re-emer- gence of coral reefs in the early Eocene during the Ceno- * Rosalía Aguilar‑Medrano [email protected] zoic climatic optimum (about 50 My) and the explosion of these ecosystems that continued into the Neogene. With 1 Department of Ecology and Evolutionary Biology, University the closure of the Tethys about 18–19 My and the diver- of California, Los Angeles, 621 Charles E. Young Dr. South, sification of coral reefs in the tectonically dynamic area Los Angeles, CA 90095, USA between Australia and mainland Asia just prior to that time, 2 Instituto de Ecología Aplicada, Universidad Autónoma the center of diversity shifted from the Mediterranean to de Tamaulipas, 356 División del Golfo, Col. Libertad, 87029 Ciudad Victoria, Tamaulipas, Mexico the Indo-West Pacific (Williams and Duda 2008; Kiessling 2009). The Pomacentridae family is closely related to the 3 Departamento Académico de Biología Marina, Universidad Autónoma de Baja California Sur, La Paz, BCS, Mexico Indo-West Pacific (Allen and Robertson 1998; Drew and Barber 2009), which has been identified by several stud- 4 Department of Geological Sciences, Biology, and Anthropology, Indiana University, 1001 E. 10th Street, ies as an evolutionary diversity hot spot (Briggs 1992; Bloomington, IN 47405, USA 1999; Bellwood and Hughes 2001; Streelman et al. 2002; 1 3 2292 Mar Biol (2015) 162:2291–2303 Fig. 1 Geographic isolation of the Pomacentridae family in the eastern Pacific showing known occurrence records as black dots. Geological ages are indi- cated for the major geographic barriers and boxes identify island groups that are discussed in the text Williams and Duda 2008; Cowman and Bellwood 2012; species of the Atlantic, (3) local mixing of the biotas after Kulbicki et al. 2013). the isolation of the eastern Pacific (EP) by environmental Pomacentridae, a group of marine fishes found in tropi- events (e.g., El Niño and La Niña), tectonic events, specia- cal and temperate waters, is one of the most abundant fami- tion and extinction, and (4) relatively recent evolution of lies in rocky and coral reefs. They present an extraordinary endemic species in isolated or marginal environments in the diversity of habitat preferences, feeding, morphology, EP (Glynn and Ault 2000; Cowman and Bellwood 2012). behavior and color pattern (Allen and Robertson 1998). The EP is biogeographically isolated by the Isthmus of The monophyly of this family has been demonstrated by Panama and the eastern Pacific barrier (Fig. 1). The grad- both morphological (Stiassny 1981; Kaufman and Liem ual rise of the Isthmus of Panama marks the final closure 1982; Lauder and Liem 1983) and molecular analyses between the Atlantic and EP around ~3–6 My (Duque-Caro (Tang 2001; Quenouille et al. 2004; Cooper et al. 2009; 1990; Coates and Obando 1996; Glynn and Ault 2000; Frederich et al. 2013). Molecular phylogenies have found Bellwood and Wainwright 2002; Steeves et al. 2005; Bacon segregation into five clades: (1) Lepidozyginae: one mono- et al. 2015); this event leads to allopatric separation of spe- specific genus; (2) Stegastinae: eight genera; (3) Chromi- cies and, over time, to speciation. nae: three genera; (4) Abudefdufinae: one genus; and (5) The eastern Pacific barrier segregates the faunas of the Pomacentridae: 16 genera (Cooper et al. 2009; Frederich EP and the Indo-West Pacific by 5000–8000 km of deep et al. 2013). Three of these subfamilies, including seven open ocean originate ~65 My ago (Ekman 1953; Dana genera and 24 endemic species, are found in the EP, distrib- 1975; Grigg and Hey 1992; Glynn and Ault 2000; Bell- uted from Monterey Bay, California, USA (Cooper 1863), wood and Wainwright 2002) (Fig. 1). The eastern Pacific in the North to the coast of Valdivia, Chile (Pequeño et al. barrier is really a strong filter rather than an absolute bar- 2005), and in the South (Fig. 1). rier and thus is not impassable as demonstrated by close Hypotheses about the origin of the fauna in the Tropical related reef fishes species living in Indo-West Pacific and Eastern Pacific suggest three main biogeographic sources EP between which gene flow occurs (Lessios and Rob- as follows: (1) immigrants from the Indo-West Pacific fol- ertson 2006; Cowman and Bellwood 2012). The Gulf of lowing long-distance dispersal before the formation of Isth- California barrier, dominated by the long peninsula of Baja mus of Panama, (2) relict species derived from ancestral California that segregates the faunas of the Pacific Ocean 1 3 Mar Biol (2015) 162:2291–2303 2293 from the Gulf of California, began to form ~25 My ago, Size taking its present shape between 12 and 3.5 My (Holt et al. 2000; Riddle et al. 2000; Bernardi et al. 2003; Robertson The size of the 24 damselfish species in the EP was and Cramer 2009; Castillo-Páez et al. 2014). obtained from the literature (Allen 1991; Aguilar-Medrano Biogeographic analyses showed that patterns of pro- et al. 2011; 2013; Table 1). The size of the species was vincialism in Tropical Eastern Pacific differ by taxonomic calculated per provinces, and a MANOVA was performed group (Ekman 1953; Briggs 1974; Boschi 2000; Hastings using provinces as grouping factor. Finally, the relation 2000; Glynn and Ault 2000; Robertson and Cramer 2009; between size and number of species per province was Kulbicki et al. 2013). The most commonly used classifica- tested by regression. tion is from Robertson and Cramer (2009) in which they recognized three provinces based on reef and shore fishes: Biogeography the Panamic and Cortez provinces along the mainland coast, and the Ocean islands province covering the offshore The biogeographic similarity between areas within the EP islands of the Tropical Eastern Pacific. was analyzed based on species occurrence data (Table 1) Habitat, food availability, ocean temperature and produc- using two main approaches: cluster analyses and parsi- tivity strongly influence the distribution of marine organ- mony analysis of endemism (PAE). Three linkage methods isms (Grove et al. 1986). Pomacentrids species present a of cluster analysis were used: (a) Jaccard similarity and (b) wide range of habitat preferences. In the EP, damselfishes Bray–Curtis similarity, neither of which treat absences as are associated with coral and rocky reefs, rocky shores and evidence of similarity between groups and both of which kelp forests; shallow tropical or subtropical waters, main- use the average linkage method to compare the aver- land shores and islands (Clarke 1971; Grove et al. 1986; age similarity values of all segment pairs within a cluster Robertson and Allen 2015); the maximum depth at which (Clarke 1993; Kosman and Leonard 2005; Robertson and they have been recorded is 150 m (Greenfield and Woods Cramer 2009), and (c) Ward’s method, which is a clustering 1980). algorithm that optimizes based on within-group variance In this study, the geographic distribution of pomacentrid rather than raw distance (Ward 1963; Sneath and Sokal species within the EP was analyzed to elucidate the provin- 1973; Kuiper and Fisher 1975; Mojena 1977; Glynn and ciality and the history of their radiation. The questions to Ault 2000; Goswami and Polly 2010). For all methods, the be answered are: (1) which are the biogeographic provinces cophenetic correlation coefficient was used as measure of of damselfishes in the eastern Pacific, (2) where was the the goodness of fit of the dendrogram to the original data center of origin of the damselfishes of the eastern Pacific (Sokal and Rohlf 1962). All cluster analyses were com- and (3) how has the center of origin shaped the current bio- puted with the statistical package PAST, version 3.0 (Ham- diversity patterns of Pomacentridae? mer et al.
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