Mar Biol (2015) 162:2291–2303 DOI 10.1007/s00227-015-2759-9

ORIGINAL PAPER

Adaptive radiation of damselfishes (Perciformes, ) 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 Duda2008 ; 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 Robertson1998 ; 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;

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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. 2001). PAE is a parsimony-based tree algorithm that builds area cladograms from distribution data and is used to Materials and methods study historical relationships between areas and the evolu- tion of endemics (Rosen 1988; Cracraft 1991, 1994; Mor- Distribution data rone and Crisci 1995; De Grave 2001), in which sympa- try may indicate a shared biological history (Morrone and A matrix of geographic occurrences of the 24 pomacen- Crisci 1995; Rosen 1988; Huang et al. 2010). PAE is one trid species from the EP was constructed based on the of the most widely used methods for describing biogeo- published literature (Allen 1991; Aguilar-Medrano et al. graphic patterns using presence/absence characters (Agui- 2011; 2013; Robertson and Allen 2015). To geographically lar–Aguilar et al. 2003; Riddle and Hafner 2006; Agui- segregate the EP, we use the 14 Tropical Eastern Pacific lar–Aguilar et al. 2005; Contreras-Medina et al., 2007; regions proposed by Glynn and Ault (2000) based on coral Casagranda et al.2012; Mavrodiev et al. 2012; Szumik reef distribution: (1) GOC, Gulf of California; (2) REV, et al. 2012) in spite of the criticism of hierarchical meth- ; (3) MXM, Mexican Province; (4) ods (Aagesen et al. 2009; Arias et al. 2010; Casagranda CLP, Clipperton island; (5) GUA, Guatemala; (6) SAL, El and Grosso 2013). Biogeographic analysis was carried out Salvador; (7) NIC, Nicaragua; (8) COC, Cocos island; (9) with TNT version 1.1 (Goloboff et al. 2003), which cal- CRC, Costa Rica; (10) GAL, Galapagos islands; (11) PAN, culates all possible most parsimonious trees, a maximum Panama; (12) MAL, Malpelo island; (13) COL, Colombia; of 100 trees saved per replicate, with 100 random addition and (14) ECD, Ecuador, and three extra regions were added replicates, using tree bisection and reconnection (TBR) as to cover all the damselfish distribution: (15) CP, California search strategy. All characters were treated as disarranged, Province; (16) PRU, Peru; and (17) CHL, Chile (Table 1). and no weighting procedure was performed. Bootstrap

1 3 2294 Mar Biol (2015) 162:2291–2303 5 1 4 7 4 1 3 1 2 7 3 3 3 1 1 2 5 Total cover Total 10 13 16 14 13 13 13 0 CHL 0 0 0 0 0 0 0 0 0 0 0 0 4 0 1 1 0 1 0 0 0 0 1 0 0 PRU 0 1 0 0 1 1 0 0 0 0 0 0 8 1 1 1 0 0 0 0 0 0 1 1 0 0 1 0 0 1 1 0 0 0 0 0 0 1 1 1 0 0 0 0 1 1 1 1 ECD 10 1 COL 0 1 0 0 1 1 0 0 0 0 0 0 8 1 0 0 0 0 0 0 1 1 0 1 0 PAN 0 1 1 0 1 1 0 0 0 0 0 0 8 1 0 0 0 0 0 0 1 1 0 1 Peru, CHL Chile 1 CRC 0 1 0 1 1 1 0 0 0 0 0 0 9 1 0 0 0 0 0 0 1 1 0 1 0 NIC 0 1 0 1 1 1 0 0 0 0 0 0 8 1 0 0 0 0 0 0 1 1 0 1 0 SAL 0 1 0 1 1 1 0 0 0 0 0 0 8 1 0 0 0 0 0 0 1 1 0 1 0 GUA 0 0 0 1 1 1 0 0 0 0 0 0 7 1 0 0 0 0 0 0 1 1 0 1 0 0 0 0 1 1 1 1 0 1 0 0 1 1 0 0 1 0 0 0 1 1 0 1 MXM 11 0 0 0 0 1 1 1 1 0 1 0 1 1 1 0 0 1 0 0 1 1 1 0 1 GOC 13 0 CP 0 0 0 0 0 1 1 0 0 0 0 0 4 0 0 0 0 0 1 1 0 0 0 0 Ecuador, PRU COL Colombia, ECD Ecuador, Panama, 1 0 1 1 0 1 1 0 1 0 0 0 1 1 0 0 0 0 0 0 1 1 1 1 GAL 12 1 0 1 1 0 0 1 0 0 0 0 0 1 1 0 0 0 0 0 0 1 1 1 1 MAL 10 0 1 1 0 1 1 0 0 0 0 0 1 1 0 0 0 0 0 0 1 1 0 1 1 COC 10 CLP 1 0 0 0 0 1 0 0 0 0 0 1 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 0 1 1 1 1 1 0 0 1 0 0 0 1 1 0 0 0 Localities REV 12 SL B (cm) 13 19 17 18 15 23 17 16 13 17 15 15 – 13 19 28 12 11 25 36 31 31 30 18 16 SL A (cm) 8 13 11 13 11 13 12 10 10 13 12 10 – 8 13 16 11 10 19 20 21 18 22 12 11 n 3 7 6 7 15 10 12 5 10 8 10 7 – 15 10 5 6 12 11 12 9 20 7 15 10 El Salvador, NIC Nicaragua, CRC Costa Rica, PAN Guatemala, SAL El Salvador, Geographic distribution of the Pomacentridae family in the eastern Pacific of the Pomacentridae family Geographic distribution maximum standard length reported by Allen ( 1991 ) SL B maximum standard length reported by standard length of the fishes used in this study, n number of specimens, SL A average 1 Table 0 indicates absence and 1 presence GOC Gulf of California, MXM Islands, CLP Clipperton Island, COC Cocos MAL Malpelo GAL Galapagos CP California province, Localities codes: REV Revillagigedo GUA province, Mexican Species baldwini Stegastes Abudefduf concolor Abudefduf Stegastes beebei Stegastes Abudefduf declivifrons Abudefduf Stegastes flavilatus Stegastes Abudefduf troschelii Abudefduf Stegastes leucorus Stegastes eupalama Stegastes rectifraenum Stegastes Azurina hirundo Stegastes redemptus Stegastes alta Chromis Total Chromis atrilobata Chromis Chromis crusma Chromis Chromis intercrusma Chromis Chromis limbaughi Chromis Chromis meridiana Chromis Chromis punctipinnis Chromis Hypsypops rubicundus bairdii Microspathodon Microspathodon dorsalis Microspathodon Nexilosus latifrons Nexilosus Stegastes acapulcoensis Stegastes Stegastes arcifrons Stegastes

1 3 Mar Biol (2015) 162:2291–2303 2295 was conducted with 1000 replicates. Consistency index The PAE results were highly similar regardless of root- (CI), retention index (RI) and bootstrap replicate values ing factor. Using GAL, we found seven most parsimonious were used as measure of goodness of fit of the area trees trees, ten using PAN and 11 using the hypothetical root. to the data. As recommended for PAE analyses, our over- The shortest trees rooted with both GAL and the hypo- all analysis was rooted with a hypothetical biogeographic thetical ancestor were 41 steps long, 40 using PAN as the ancestor of all zeros (absence; Morrone and Crisci 1995). root. The ensemble consistency index (CI) using GAL and To further test the biogeographic relationship between the the hypothetical root is 0.61, and 0.62 using PAN. The EP damselfish with the Indo-West Pacific and Atlantic, we trees rooted with the hypothetical root yielded the highest used two additional rooting relationships: (a) the relation- ensemble retention index (RI): 0.75, while GAL yielded ship with the Atlantic using Panama as the root and (b) the the lowest: 0.71 and PAN was intermediate at 0.73. Two relationship with the Indo-West Pacific using Galapagos clusters were conserved in all three analyses: (1) North Islands as the root. (GUA, MXM, GOC, REV), which give the highest boot- strap values using PAN as rooting factor; and (2) EP equa- torial islands (GAL, COC, MAL), whose highest bootstrap Results values were with the hypothetical root (Fig. 3). Based on the combined results (cluster and PAE), Pomacentridae provinciality in the eastern Pacific we recognize six provinces for damselfishes of the east- ern Pacific. (1) EPEI: EP equatorial islands (GAL, MAL, All cluster analyses produced dendrograms with six main COC) recovered in all analyses (clustering and PAE). groups (Fig. 2): (1) the outlying localities in the extreme (2) N: North (GUA, MXM, GOC, REV) recovered in all North (CP), South (CHL) and West (CLP); (2) oceanic analyses (clustering and PAE); the inclusion of GUA in islands and mainland Mexico (MXM, GOC, REV); (3) the this cluster is supported by all PAE analyses. (3) Center southern localities (ECD and PRU); (4) southern Central (SAL, NIC, PAN, CRC, COL), which is recovered in all America (PAN, CRC, COL): (5) Central America (GUA, the cluster analyses, but which is not recovered as a group SAL, NIC); and (6) EP equatorial islands (GAL, COC, in the PAE consensuses trees shows the central localities MAL). However, using Jaccard and Bray–Curtis similar- as non-group to any cluster. Cluster analyses recognize ity, PAN is always basal to the central localities (GUA, the southern localities as one subgroup (ECD, PRU) and SAL, NIC, CRC, COL). The cophenetic correlation coef- extreme localities as another (CHL, CP, CLP), while PAE ficient was higher using Jaccard and Bray–Curtis similarity analyses using GAL and PAN as rooting factors lumped (0.951). the two subgroups into one (ECD, PRU, CHL, CP, CLP).

Fig. 2 Cluster of the localities of distribution of the damselfishes in CRC, Costa Rica; GAL, Galapagos islands; PAN, Panama; MAL, the eastern Pacific using three linkage methods: Ward, Bray–Curtis Malpelo island; COL, Colombia; ECD, Ecuador; CP, California Prov- and Jaccard. Localities: GOC, Gulf of California; REV, Revillagigedo ince; PRU, Peru; CHL, Chile. Coph. corr.: cophenetic correlation islands; MXM, Mexican Province; CLP, Clipperton island; GUA, coefficient Guatemala; SAL, El Salvador; NIC, Nicaragua; COC, Cocos island;

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Fig. 3 Parsimony analysis of endemicity of Pomacentridae family Mexican Province; CLP, Clipperton island; GUA, Guatemala; SAL, in the eastern Pacific. a Tree using a constructed root, b tree using El Salvador; NIC, Nicaragua; COC, Cocos island; CRC, Costa Rica; Panama as rooting factor, c tree using Galapagos as rooting factor, d, GAL, Galapagos islands; PAN, Panama; MAL, Malpelo island; COL, e, f consensus trees of a, b and c. Numbers in the branches of a, b and Colombia; ECD, Ecuador; CP, California Province; PRU, Peru; CHL, c: bootstrap values. Numbers in the branches of d, e and f: branch Chile length. GOC, Gulf of California; REV, Revillagigedo islands; MXM,

(4) South (ECD, PRU, CHL), including CHL, and extreme of damselfish found in the EP are found in any other ocean; localities. (5) Clipperton. (6) California Province (Table 2). thus, the endemism in the EP at the species level is 100 % Provinces 4, 5 and 6 are geographically coherent, and all and close to 50 % at the generic level, with three endemic three were recovered in the PAE tree rooted with the hypo- genera: Azurina, Nexilosus and Hypsypops. The gen- thetical ancestral area. A map showing the six provinces for era with the largest distribution are Chromis (100 % of damselfishes of the eastern Pacific, with additional infor- the sites), Abudefduf, Stegastes (94.12 % of the sites) and mation about temperature (Levitus and Boyer 1994), major Microspathodon (76.47 % of the sites). The species that are sand gaps (Robertson and Cramer 2009) and productivity most widely distributed in the EP are A. troschelii (94.12 % (chlorophyll a concentrations; Capone and Hutchins 2013), of the sites), Ch. atrilobata (88.24 % of the sites), M. bair- was used to visualize biogeographic patterns of the eastern dii, M. dorsalis, S. acapulcoensis and S. flavilatus (76.47 % Pacific (Fig. 4). of the sites). Ten species have restricted distributions (i.e., species that occur in less than 18 % of the sites). We cat- Patterns of distribution egorized these species into two progressively restricted groups: (1) endemic species: species found in two or three The geographic distribution of damselfishes in the EP cov- localities: Ecuador, Peru and Chile, Ch. crusma and Ch. ers a large area, from Monterey Bay, California, USA (36° intercrusma; Revillagigedo, Gulf of California and Mexi- 36′ 22″N, 121° 52′ 13″W; Cooper 1863), in the North to can Province, Ch. limbaughi and S. rectifraenum; Gulf of the coast of Valdivia, Chile (39° 51′ 12″S, 73° 23′ 56″W; California and California Province, H. rubicundus; Gulf Pequeño et al. 2005), and in the South, approximately of California and Revillagigedo islands, S. redemptus, and 9860 km longitudinally (Figs. 1, 5). None of the 24 species (2) microendemic species: those species present at only

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Table 2 Localities, provinces Localities Abrev. Province Abrev. Size (cm) Spp. number and variables Guatemala GUA North N Mean 13.1 14 Mexican Province MXM Max. 21.43 Gulf of California GOC Min. 8.13 Revillagigedo islands REV El Salvador SAL Center C Mean 13.57 10 Nicaragua NIC Max. 21.43 Panama PAN Min. 8.13 Costa Rica CRC Colombia COL Galapagos islands GAL Eastern Pacific EPEI Mean 13.73 12 Malpelo island MAL Equatorial islands Max. 22.4 Cocos island COC Min. 8.13 Ecuador ECD South S Mean 15.07 10 Peru PRU Max. 22.4 Chile CHL Min. 8.13 California Province CP California CP Mean 15.93 4 Province Max. 19.76 Min. 11.5 Clipperton CLP Clipperton CLP Mean 10.41 3 Max. 13.17 Min. 7.79

Abrev abbreviation one locality: California Province, Ch. punctipinnis; Revil- and EPEI (mean 13.73 cm; max 22.40 cm; min 8.13 cm; lagigedo islands, A. hirundo; Clipperton, S. baldwini; and n 142 organisms), while CLP presents the lowest val- = Galapagos, A. eupalama. The species with restricted distri- ues (mean 10.41 cm; max 13.17 cm; min 7.79 cm; n 24 = butions are principally found in islands or at the extremes organisms). The MANOVA of size shows significant dif- of the Pomacentridae distribution (Fig. 5). ferences between provinces (F 3.82; p < 0.002), 5–651 = Considering species richness at the locality level, the specially between three groups: (1) CLP, (2) CP and (3) S, islands with the highest number of species are: Galapa- N, C, EPEI. Number of species per province show no sig- gos, Revillagigedo (12 species each), Cocos and Malpelo nificant relation to size (r2 0.09; p 0.08); this result = − = (10 species each). The mainland coastal localities with the could be related to the fact that areas with higher number highest number of species are: The Gulf of California (13 of species present the biggest and smallest species due to species), Mexican Province (11 species) and Ecuador (10 a wider range of sizes, while the areas with few number of species) (Fig. 5). species present the intermedium values (see Table 2).

Size variation Discussion The mean standard length for damselfishes from the EP is 13.39 cm; the species with the longest mean are N. lati- One goal of biodiversity sciences is to understand the his- frons (mean 22.40 cm) and M. bairdi (mean 21.43 cm), torical phases that a group in developing its present pat- while species with the smallest mean are S. baldwini (mean terns of diversity. Reef fish are an important group of more 7.79 cm) and Ch. atrilobata (mean 8.13 cm; Table 1). than 5000 species (Bellwood et al. 2010), and damself- Using provinces as grouping factor, the largest damself- ishes are the third largest reef fish group, with 394 species ish are found in CP (mean 15.93 cm; max 19.76 cm; min (Eschmeyer 2015). Most damselfishes inhabit the central 11.50 cm; n 49 organisms) and South (mean 15.36 cm; Indo-Australian Archipelago (60 %), and the EP damself- = max 22.40 cm; min 10.24 cm; n 140 organisms); the ish community is thus smaller than the communities in = mean values are registered for Center (mean 13.57 cm; max any other sea (Atlantic, Indian Ocean, Central Pacific and 21.43 cm; min 8.13 cm; n 128 organisms), North (mean Indo-Australian Archipelago; Cowman and Bellwood = 13.10 cm; max 21.43 cm; min 8.13 cm; n 174 organisms) 2012). However, the biogeographic characteristics of the = 1 3 2298 Mar Biol (2015) 162:2291–2303

Fig. 4 Biogeographic provinces of damselfishes of the eastern Pacific indicating major eco- logical barriers as: superficial water temperature (Levitus and Boyer, 1994), sand gaps (Rob- ertson and Cramer, 2009) and areas of maximum concentra- tion of chlorophyll a (Capone and Hutchins, 2013)

Fig. 5 Connection web for the six biogeographic provinces of the Pomacentridae family in the eastern Pacific. EPEI, EP equatorial islands; S, South; CP, California Province; CLP, Clipperton island; C, center; N, North. a Diversity. Numbers in parentheses indicate the number of species in each region. Colors represent genera, and the size of each slice is proportional to the number of species. b Endemicity and interconnec- tions. Numbers report the shared species between provinces. Colors represent genera and the size of each slice is proportional to the number of endemic spe- cies per genus

EP community make it especially interesting due to: (1) endemic and (2) physical conditions; most of the eastern endemicity; three of the seven genera (Azurina, Hypsypops Pacific environments are influenced by temperate currents, and Nexilosus) and 100 % of the species of the area are which favor rocky reefs or kelp forest over coral reefs.

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Thus, it is of special interest to understand the patterns of At one time, damselfishes had colonized the central area diversification of damselfish in the eastern Pacific, which (EPEI and Central) by immigration from the Indo-West might be a key to understanding the worldwide radiation of Pacific; relict species derivate from the ancestral connec- this fish family. tion with the Atlantic and local mixing (Glynn and Ault 2000; Cowman and Bellwood 2012). They then spread both Diversification in the eastern Pacific to the North (REV, GUA, MXM, GOC) and South (ECD, PRU, CHL). Both these areas have different physical con- The number of provinces in the Tropical Eastern Pacific ditions that impact distributions. The North and the South has been studied intensively, but with little resolution as have fewer coral reefs and are dominated by rocky reefs the classification depends strongly on which group is being and kelp forest (Steneck et al. 2002). Both regions are influ- analyzed, suggesting that the ecology and biogeography enced by temperate currents: the California Current in the of the eastern Pacific are not governed by overarching fac- North and the Humboldt Current in the South. And in these tors that apply to all taxa. Each group may respond to the regions occur some of the most important upwelling areas complex of eastern Pacific factors differently. Indeed, the of the eastern Pacific (Capone and Hutchins 2013; Fig. 4). factors that are important in the distribution of the reef fish The conditions of these areas (especially CP, PRU, CHL) communities differ from analysis to analysis. For example, are thus highly different from the Central Province, and the two stretches of sand and mud shorelines, the Sinaloan diversification in these latitudinally extreme areas is limited Gap (370 km of shoreline) and the Central American Gap (CP and CHL host only four species each). Damselfish spe- (~1000 km of shoreline; Robertson and Cramer 2009), cies inhabiting these localities are mainly endemic, three were identified as important factors in the provincial clas- Chromis species in the South (ECD, PRU, CHL) and six sifications by Ekman (1953), Walker (1960) and Hastings species of Chromis, Hypsypops, Azurina and two Stegastes (2000), but not in the classifications of Briggs (1974), in the North (REV, GOC, MXM, GUA). Boschi (2000), Spalding et al. (2007), Robertson and Kelp forests found in shallow rocky coasts and cold Cramer (2009) or our analyses (Fig. 4). Water temperature temperate waters are generally diverse and productive eco- fluctuates considerably over time and space in the EP. The systems (Mann 1973; Stephens et al. 2006). However, few latitudinal range from equatorial to temperate regions varies damselfish populations persist in these environments. In the greatly due to climate events such as El Niño and La Niña North, species as Hypsypops rubicundus and Chromis punc- that change the range of temperatures, the spatial range and tipinnis are two well-known kelp forest damselfish, while the speeds of the ocean currents from year to year, and the in the South there is Ch. crusma. One important adaptation seasonal upwelling systems scattered throughout the region of damselfishes to these environments was increase in body (Glynn and Ault 2000; Robertson and Cramer 2009). It size. Bergmann’s rule (Bergmann 1847) posits that the body appears that the upwelling of California and Ecuador may size of an should be larger in colder climates (poles, be important in defining the extreme North and South dis- higher latitudes). This rule holds for damselfishes from the tribution of damselfishes, probably due to food availability EP. One of the classic explanations of the Bergmann rule (Fig. 4). in ectotherms is that at relatively lower temperatures ecto- The EP equatorial islands (GAL, COC, MAL) are influ- therms typically mature later and thus at larger sizes than enced by three major ocean currents: the southern area of conspecifics at higher temperatures (Ray 1960; Atkinson these islands receives the temperate Humboldt Current, 1994; Sibly and Atkinson 1994). In this particular study, the northern receives the moderately warm North Equato- the size-temperature relationship also could be related to rial Current and the Equatorial undercurrent causing a cold the increased swimming cost on temperate environments, upwelling rich in nutrients near the western shores (Car- which may be offset by higher energy reserves afforded by rasco 2000). The central localities (SAL, NIC, PAN, CRC, large body fishes. Potentially allowing damselfishes in these COL) are mainly affected by the Contra and North Equato- demanding habitats to swim for longer periods of time. rial currents, with higher water temperatures than the EPEI. The Gulf of California, which is part of the North prov- Our analyses show that the EPEI and the Central Province ince, presents favorable conditions for the development share nine species, of which six are widely distributed in of marine life and is home to the highest number of dam- the EP and one is endemic to the EPEI. The Central Prov- selfishes in the EP (13 species). The Gulf of California ince has no endemic species. The Central Province appears has been recognized as one of the most diverse and unique to have fewer barriers to dispersal due to its environment ecosystems on the world, comprising a macrofauna of conditions as similar temperature in the whole area as well approximately 5969 species, 4854 invertebrates and 1115 as no physical barriers and thus functions as an area of vertebrates from where 891 are fishes and from these 77 are overlap or a corridor from Galapagos to the Gulf of Cali- endemic (Brusca et al. 2005; Lluch-Cota et al. 2007). This fornia, the two areas with the largest number of species. diversity may be related to protection from heavy swell

1 3 2300 Mar Biol (2015) 162:2291–2303 provided by the semi-enclosed area, to the highly complex did ours, two centers of species richness, one subtropical structure of habitats (Munday and Jones 1998; Robertson and the other equatorial (Glynn and Ault 2000; Robertson and Cramer 2009), to its high productivity (Capone and and Cramer 2009). In our study, the subtropical center of Hutchins 2013), and to the grading of temperature and the species richness is the Gulf of California, while the equa- habitat heterogeneity from its subtropical southern mouth, torial center of species richness is Galapagos Islands. In which support coral reefs, to its temperate northern head the North Province, the Gulf of California has the highest with rocky reefs (Robertson and Cramer 2009). diversity of damselfish species (13 of 24 species), of which Clipperton Island has the most remote reefs of the EP, six are widely distributed species (present in 13–16 of the located 1.110 km southwest of the Mexican coast and 17 total localities) and three species are endemic (defined 950 km South of Revillagigedo Islands. Clipperton has the here as species present in two to three of the 17 localities), largest coral reef in the EP and is strongly influenced by the while the equatorial center of species richness, Galapagos warm waters of the North Equatorial Current (Robertson Islands, has 12 species, six are widely distributed species and Allen 1996). Clipperton shares one wide distributed and one microendemic species (defined here as species pre- species (Abudefduf troschelii) with most other EP locali- sent in only one locality). Both centers of richness have (1) ties, one species with the North province (Chromis alta), high diversity, (2) closeness of phylogenetic relationships and has one endemic species (Stegastes baldwini). Revil- among taxa, (3) sympatric speciation and (4) phylogeneti- lagigedo Islands, the closest habitat to Clipperton, host cally young species. four of the eight species of the genus Stegastes, and the However, our analyses provide support for the Central occurrence of S. baldwini at Clipperton may be the result Province as the center of origin of eastern Pacific poma- of peripheral speciation from Revillagigedo islands; how- centrids based on bootstrap values, even though it is not a ever, to prove this point a good phylogeny is needed. Also, center of richness. The Central Province (SAL, NIC, CRC, while Clipperton Island is a tropical area with high coral PAN, COL) has medium richness made up of non-endemic cover whose conditions could support many more species, species (Fig. 5). Richness and endemicity increase to the the low number of species there could be the result of (1) North (GUA, REV, MXM, GOC) and in the EP equatorial habitat/food availability, since the island is small (6 km2, islands (GAL, COC, MAL). However, the central locali- Robertson and Allen 1996). Habitat and food availability ties share the largest number of species with EP equatorial have shown to be important variables to explaining recent islands, North and South (Fig. 5). The Equatorial Contra shifts or contractions/expansion in the ranges of distribu- Current favors the dispersion of larvae from the Central tion (Fenberg et al. 2014; McCabe and Olson 2015), and Province and EP equatorial island to the North through the (2) geographic distance between the island and the main- North Equatorial Current and the South through the South land, which constitutes a potential barrier to dispersal and Equatorial Current (Grigg and Hey 1992; Lessios and gene flow (Muss et al. 2001). Robertson 2006; Robertson and Cramer 2009; Wood et al. While diversity in islands is limited by the distance to 2014). The Central Province also is home to the four genera the mainland and the area of the island, as was observed in with the widest distribution (Abudefduf, Chromis, Micro- the Clipperton fauna, in continental areas ocean tempera- spathodon, Stegastes), all of which have closely related ture can often be the limiting factor, as observed in Chile species in the west Atlantic (ATL), including A. troschelii and California Province, where temperate ocean currents (EP) and A. saxatilis (ATL), which, based on holoenzymes, create environments where only a few damselfish, most diverged only 5.8 My (Gorman and Kim 1977), Ch. atri- of them endemic, can survive and persist. In these temper- lobata (EP) and Ch. multilineata (ATL), which, using ate environments damselfish tend to be larger and stouter, hypervariable portion of the mitochondrial control region characters that allow them to amass energy reserves to deal (D-loop), diverged 0.93–3.26 My (Domingues et al. 2005), with the low temperatures. and M. dorsalis (EP) and M. chrysurus (ATL) which, using nuclear and mitochondrial gene fragments, diverged Center of origin versus center of richness approximately 6–7 My (Frederich et al. 2013), all consist- ent with the final closure of the Isthmus of Panama around It has been hypothesized that the centers of origin and 3–6 My (Duque-Caro 1990; Coates and Obando 1996; speciation present general characteristics such as: (1) Glynn and Ault 2000; Bellwood and Wainwright 2002; high diversity, (2) closeness of phylogenetic relationships Steeves et al. 2005; Bacon et al. 2015). among taxa, (3) sympatric speciation, and (4) phylogeneti- In summary, our results reveal the radiation of Poma- cally young species (McManus 1985; Briggs 1999; 2003; centridae in the eastern Pacific to be a dynamic disper- Mora et al. 2003). This model of centers of origin thus sup- sion system, whose history can be segregated into three poses that they are also centers of richness. Previous bio- main steps: (1) mixture and speciation of species with geographic analyses of the eastern Pacific have found, as close affinity to west Atlantic ancestral stocks in the

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