Chrysiptera, Swainson, 1839

Tang, Kevin L., Stiassny, Melanie L. J., Mayden, Richard L. & DeSalle, Robert, 2021, Systematics of Damselfishes, Ichthyology & Herpetology 109 (1), pp. 258-318 : 290-293

Chrysiptera .

— There are 40 currently recognized species of Chrysiptera found throughout the Indo-West Pacific. Allen (1975a) split the genus into two broad complexes. The one that included C. biocellata , C. glauca , C. leucopoma , C. niger , and C. unimaculata was united by fin-ray and gill-raker counts, extent of predorsal scalation, lack of preorbital and suborbital (i.e., infraorbital) scalation, elongate teeth, similar head shape, and continuous dorsal-fin profile. The other complex, with C. hemicyanea , C. oxycephala , C. rollandi , C. talboti , and C. traceyi , displayed fewer dorsal- and pectoral-fin rays, less elongate teeth, a distinctive dorsal-fin profile with deeply incised membranes between anterior dorsal spines, and a prominent notch between the spinous and soft portions of the dorsal fin. He was unsure about the affinities of C. caeruleolineata , C. cyanea , C. flavipinnis , C. rex , and C. tricincta . He suggested that C. galba , C. notialis , C. rapanui , and C. starcki may be related, but did not speculate as to their relationship to other Chrysiptera . Allen (1975a: 42) warned that this diverse genus, then called Glyphidodontops , probably was not monophyletic, remarking that it presented ‘‘some of the most serious problems for students of pomacentrid taxonomy.’’ This statement remains true today. Hensley (1978: 15) referred to it as a catch-all genus, one that ‘‘is likely to be separated into other genera after detailed studies.’’ Allen (1987b: 109) concurred, saying that it ‘‘may ultimately be split into several genera.’’ Doubts about its monophyly were reiterated in his later works (Allen and Adrim, 1992; Allen, 1999b; Allen and Erdmann, 2008b; Allen et al., 2010b, 2015b). Quenouille et al. (2004) published the first molecular phylogeny with significant sampling within Chrysiptera and confirmed the disarray by recovering putative Chrysiptera in three different lineages. Subsequent studies (Cooper et al., 2009; Cowman and Bellwood, 2011; Hubert et al., 2011, 2012, 2017; Hofmann et al., 2012; Litsios et al., 2012a, 2012b; Frédérich et al., 2013; Rabosky et al., 2013, 2018; Lobato et al., 2014; DiBattista et al., 2016; Mirande, 2016; Gaboriau et al., 2018; Delrieu-Trottin et al., 2019) have further reinforced this, finding species of Chrysiptera scattered across the Pomacentrinae . Chromosomal variation hinted at this polyphyly. Takai and Ojima (1995) commented that ‘‘ Chrysiptera may be one of the genera in which the karyotypes have altered most actively in Pomacentridae ,’’ a statement that was made under the assumption of its monophyly. Differences in early development among putative Chrysiptera also suggested that the genus was not monophyletic (R. E. Thresher, pers. comm.).

The results of this analysis agree with recent phylogenies: Chrysiptera , in its current state, is broadly polyphyletic. The putative species of Chrysiptera are distributed in several disjunct lineages, most of which are confined to the tribe Cheiloprionini ( Fig. 1 ). The remaining ‘‘ Chrysiptera ’’ are paraphyletic relative to Amblypomacentrus , in the tribe Pomacentrini . Because the putative species of Chrysiptera are dispersed across the subfamily Pomacentrinae , we hereby restrict Chrysiptera sensu stricto to the clade that encompasses the following species: C. caesifrons , C. chrysocephala , C. cyanea (type species), C. hemicyanea , C. oxycephala , C. parasema , C. rex , C. rollandi , C. springeri , C. talboti , and C. taupou . This assemblage contains the majority of bright blue species (e.g., C. cyanea , C. hemicyanea , C. springeri ) and is sister to Cheiloprion . Chrysiptera sensu stricto is equivalent to ‘‘ Chrysiptera I’’ of Quenouille et al. (2004: fig. 2), ‘‘ Chrysiptera 2’’ of Cooper et al. (2009: fig. 2), ‘‘ Chrysiptera Clade II’’ of Cowman and Bellwood (2011: figs. 2b, S6), and a clade within ‘‘ Chrysiptera II’’ of Frédérich et al. (2013: 98). A group comprising some combination of these species has been recognized in the literature. Allen and Lubbock (1976) characterized C. hemicyanea , C. oxycephala (as Glyphidodontops azurepunctatus ), C. rollandi , C. springeri , C. talboti , and C. traceyi by their deeply incised spinous dorsal-fin membrane, similar dentition, lower meristic counts (viz., soft dorsal, anal, and pectoral rays), and deeper, more ovate body compared to congeners. Allen (1987b) also made note of the deeper body and incised spinous dorsal fin when grouping together C. hemicyanea , C. oxycephala , C. sinclairi , and C. springeri . Allen and Adrim (1992) and Allen (1999b) added C. pricei and C. cymatilis , respectively, to the species complex on the basis of those features. Allen and Erdmann (2008b) named it the ‘‘ hemicyanea complex’’ when they added the newly described C. giti . Subsequently, Allen et al. (2010b, 2015a, 2017a, 2018a) expanded the complex to include C. arnazae , C. burtjonesi , C. ellenae , C. maurineae , C. papuensis , and C. uswanasi . Within this hemicyanea complex, Allen et al. (2015a) further demarcated a ‘‘ Chrysiptera oxycephala species complex’’ that consisted of C. ellenae , C. maurineae , C. oxycephala , C. papuensis , and C. sinclairi . Allen et al. (2017a, 2018a) recently added a sixth, C. burtjonesi , and seventh representative, C. uswanasi .

The phylogenetic relationships within Chrysiptera sensu stricto produced by this analysis show three distinct clades, a result which largely agrees with earlier works. One clade includes a sister-group pairing of C. cyanea and C. taupou ( Randall et al., 1997; Randall, 2005) plus a monophyletic C. rex complex (Allen et al., 2015b). Drew et al. (2010) first detected genetic variation within C. rex that corresponded to regional color morphs. Allen et al. (2015b) described this cryptic diversity as a ‘‘ Chrysiptera rex species complex’’ composed of C. caesifrons , C. chrysocephala , and C. rex . Steinke et al. (2009) recorded genetic divergence within C. cyanea , which may also represent undescribed diversity. They reported a clear break between COI sequences of Indonesian C. cyanea and those from the Philippines. They proposed resurrecting Chrysiptera punctatoperculare for the population in the South China Sea. However, C. punctatoperculare was not described from the Philippines, instead coming from the Ryukyu Islands in the neighboring East China Sea ( Fowler, 1946). Furthermore, there are other junior synonyms of Chrysiptera cyanea described from the Philippines ( Glyphidodon assimilis , Abudefduf turchesius , and Abudefduf sapphirus ) that have seniority over C. punctatoperculare and could have priority instead. More detailed examination will be necessary to resolve this nomenclatural issue if additional species are recognized within C. cyanea . A second clade within Chrysiptera sensu stricto includes C. rollandi , C. talboti , and C. traceyi (Allen, 1975c) . The third clade includes the hemicyanea complex (Allen and Erdmann, 2008b; Allen et al., 2010b), which contains C. oxycephala . The composition of these three clades is consistent with other pomacentrid phylogenies ( Quenouille et al., 2004; Cooper et al., 2009; Cowman and Bellwood, 2011; Litsios et al., 2012b; Lobato et al., 2014; Mirande, 2016; Delrieu-Trottin et al., 2019), though the interrelationships between them do vary from one study to the next. Based on control region data (Allen et al., 2010b, 2015a, 2017a, 2018a), the following species also should be considered part of Chrysiptera sensu stricto: C. arnazae , C. burtjonesi , C. ellenae , C. giti , C. maurineae , C. papuensis , C. sinclairi , and C. uswanasi . Following remarks in the literature (Allen and Adrim, 1992; Allen, 1999b; Allen et al., 2003, 2010b; Allen and Erdmann, 2008b, 2012), we provisionally designate C. cymatilis and C. pricei as members of Chrysiptera sensu stricto. If these assignments are correct, this newly reorganized genus would include more than half (22) of the species formerly classified in Chrysiptera .

The remaining ‘‘ Chrysiptera ’’ in the Cheiloprionini present taxonomic challenges that cannot be resolved herein. We recovered a clade composed of C. galba , C. rapanui , and C. starcki (100% bootstrap) as the sister to another group of ‘‘ Chrysiptera .’’ Prior studies have linked C. galba and C. rapanui with a third species, C. notialis (Allen and Randall, 1974; Allen, 1975a, 1975c). All four species occur along southern Oceania, with all but C. starcki restricted to the Southern Hemisphere (Allen, 1973b, 1975a, 1975c; Allen and Randall, 1974); ‘‘ Chrysiptera ’’ starcki appears to have an antiequatorial distribution (Allen, 1975a; Ida and Moyer, 1975; Randall, 1981). For the purposes of our discussion, we refer to this clade as the Oceanic ‘‘ Chrysiptera ’’ for their geographic distribution. They are united by the condition of their teeth: ‘‘All except G. rapanui have uniserial teeth, which is atypical for Glyphidodontops ’’ (Allen, 1975a: 42). The position and relationships of these species vary greatly among molecular phylogenies. Quenouille et al. (2004) were the first to sequence a member of this group, C. galba , and recovered it in their ‘‘ Chrysiptera II ,’’ as the sister species to C. glauca þ C. leucopoma , a relationship equivalent to the one reported herein. However, Cooper et al. (2009: 14) understandably questioned the identity of the sample because Quenouille et al. (2004: table 1) specified that it was collected from Indonesia, well outside of the known range of C. galba in southeastern Oceania (Allen and Randall, 1974; Allen, 1975a, 1991). Further complicating matters, the stated Indonesian provenance of that specimen (stri-x-2814) is in doubt because its GenBank entries ( AY208431 , AY208568 ) list the source as ‘‘aquarium traders.’’ In BLAST searches, the cyt b sequence ( AY208568 ) is a.99% match with published records of C. galba collected from the Gambier Islands ( KM455353 – KM455364 ) and Rapa Nui ( MK100728 ), which are within its native range (Delrieu-Trottin et al., 2014, 2019). These data strongly suggest that, despite its unclear origin, the specimen probably is C. galba . Cowman and Bellwood (2011: figs. 2b, S6), using those sequences from Quenouille et al. (2004), resolved C. galba as the sister group of Pomachromis in their ‘‘ Chrysiptera I et al.’’ Litsios et al. (2012b: figs. A1–A3) found C. galba as the sister group of either Altrichthys or a large pomacentrine clade that included genera like Amphiprion , Amblyglyphidodon , Neopomacentrus , and Pomacentrus . Rabosky et al. (2013) inferred C. galba as the sister group to a clade of Cheiloprion , Chrysiptera sensu stricto, and Pomachromis . Several studies ( Litsios et al., 2012a; Frédérich et al., 2013; DiBattista et al., 2016; Gaboriau et al., 2018) have examined both C. galba and C. starcki but failed to recover them together. Litsios et al. (2012a) showed C. galba as sister to Pomachromis but grouped C. starcki with Nexilosus in a clade sister to the rest of Pomacentrinae . Frédérich et al. (2013) found C. starcki (part of their ‘‘ Chrysiptera I’’) sister to Pomachromis and C. galba (part of their ‘‘ Chrysiptera II’’) sister to Cheiloprion . DiBattista et al. (2016) resolved C. galba as the sister species of a clade equivalent to our Cheiloprionini. However, they found C. starcki as the sister group of the herbivorous ‘‘ Chrysiptera ’’ (see below). Gaboriau et al. (2018) reported the same relationship for C. starcki but recovered C. galba sister to Cheiloprion . The discordant results may be due, in part, to sequences from specimens incorrectly identified as C. galba . In addition to the sequences of C. galba from Quenouille et al. (2004), both Litsios et al. (2012a: additional file 2) and Frédérich et al. (2013: table S1) used a COI sequence ( FJ583183 ) attributed to a sample of ‘‘ C. galba ’’ collected from the Philippines, which is extralimital for C. galba , one of several deposited in GenBank ( FJ583183 – FJ583187 ). DiBattista et al. (2016: appendix S1) used another COI sequence ( FJ583184 ) from the Philippines to represent C. galba . Gaboriau et al. (2018) looked at another barcode sequence from the Philippines ( FJ583187 ). Rabosky et al. (2018: Dryad files ‘‘accession_numbers.csv’’, ‘‘dropped_ rogues.csv’’) also examined FJ583183 but identified C. galba as a rogue taxon before pruning it from their analyses. They resolved C. starcki as the sister group to the rest of the Pomacentrinae . Delrieu-Trottin et al. (2019) generated novel DNA sequences for C. galba and C. rapanui . They recovered both species with C. starcki . In finding a group composed of C. galba , C. rapanui , and C. starcki , our result is consistent with Delrieu-Trottin et al. (2019) and traditional classifications (Allen and Randall, 1974; Allen, 1975a, 1975c). Steinke et al. (2009) detected COI sequence divergence showing a geographic divide between individuals of C. starcki from the Philippines and those from Tonga. Their finding suggests that the disjunct northern and southern populations may be different species.

The Oceanic ‘‘ Chrysiptera ’’ are sister to a monophyletic group containing C. biocellata , C. brownriggii , C. glauca , C. leucopoma , and C. unimaculata . That composition closely follows one of Allen’s (1975a) complexes. The species of this group are primarily herbivorous (Allen, 1975a; Kuo and Shao, 1991) and include all of the Chrysiptera ( C. biocellata , C. brownriggii , C. glauca , C. leucopoma , and C. unimaculata ) known to engage in algal farming (Ceccarelli, 2007; Pratchett et al., 2016). For the purposes of discussion, we will refer to this clade as the herbivorous ‘‘ Chrysiptera .’’ They usually occur in shallow waters exposed to surge and wave action, often over rubble and rocky substrates (Allen, 1975a, 1991; Masuda et al., 1984; Myers, 1999; Allen et al., 2003). The grouping recovered in our phylogeny (100% bootstrap) is equivalent to ‘‘ Chrysiptera II’’ of Quenouille et al. (2004: fig. 2), ‘‘ Chrysiptera 1’’ of Cooper et al. (2009: fig. 2), a clade within ‘‘ Chrysiptera I et al.’’ of Cowman and Bellwood (2011: figs. 2b, S6), and a clade within ‘‘ Chrysiptera I’’ of Frédérich et al. (2013: 98). The composition matches those of previous phylogenies, and the relationships among the species are mostly congruent with them as well. Masuda et al. (1984) remarked on the resemblance of C. biocellata , C. leucopoma , and C. unimaculata . All three were found together in a clade, along with C. brownriggii . The C. brownriggii – C. leucopoma sister-group relationship is expected considering C. leucopoma was, until recently, regarded as a junior synonym of C. brownriggii (e.g., Randall et al., 1997; Allen and Bailey, 2002; Quenouille et al., 2004; Randall, 2005; Cooper et al., 2009; Motomura et al., 2010). Allen et al. (2015b) resurrected C. leucopoma , removing it from the synonymy of C. brownriggii , with C. brownriggii restricted to the Indian Ocean and C. leucopoma as its sister species in the Pacific. They did so on the basis of genetic distances between the two populations first reported by Hubert et al. (2012: fig. S1, table S3).

The other lineage of ‘‘ Chrysiptera ’’ in the Cheiloprionini contains a single species, C. flavipinnis . Its phylogenetic position is highly unstable. Our phylogeny recovers it as sister to Dischistodus . However, the placement of this species is variable, with it often appearing elsewhere within Cheiloprionini , e.g., as the sister taxon of Pomachromis . DiBattista et al. (2016), the only other phylogeny to examine C. flavipinnis , found it sister to C. leucopoma . In the original description, Allen and Robertson (1974) hypothesized that it is closely related to C. cyanea but noted the lack of deeply incised membranes between the dorsal-fin spines which is characteristic of C. cyanea and other Chrysiptera sensu stricto. They also observed that this species occurs at greater depths (9.5– 37 m) than C. cyanea (, 5 m). The sequence used in this analysis was obtained from the BOLD data portal (LIFSA265- 08; UG1067; Australia: 14838 0 09.6 00 S, 145827 0 18.0 00 E) and appears to be correctly identified based on the photo of the voucher specimen available online.

The last of the putative ‘‘ Chrysiptera ’’ include C. annulata , C. kuiteri , and C. tricincta , which are the black-and-white species (footballers). These fishes are equivalent to ‘‘ Chrysiptera III’’ of Quenouille et al. (2004: fig. 2) and Frédérich et al. (2013: 98), and ‘‘ Chrysiptera 3’’ of Cooper et al. (2009: fig. 2). They are not closely related to Chrysiptera sensu stricto or the other ‘‘ Chrysiptera ’’ in the Cheiloprionini . Instead, the three species are paraphyletic relative to a monophyletic Amblypomacentrus in the tribe Pomacentrini . This Amblypomacentrus – ‘‘ Chrysiptera ’’ clade is sister to the rest of the Pomacentrini . A connection between these ‘‘ Chrysiptera ’’ and Amblypomacentrus has been discussed by other workers (Cooper et al., 2009; Cowman and Bellwood, 2011; Litsios et al., 2012a; Frédérich et al., 2013; Rabosky et al., 2013, 2018; Lobato et al., 2014; DiBattista et al., 2016; Mirande, 2016; Gaboriau et al., 2018; Delrieu-Trottin et al., 2019). Cowman and Bellwood (2011: figs. 2b, S6) labeled a similar group as ‘‘ Chrysiptera Clade III et al.’’ Frédérich et al. (2013) called it ‘‘ Chrysiptera III þ Amblypomacentrus clarus .’’ Similarities in coloration between these species have been noted in the literature ( Randall et al., 1997: 252; Cooper et al., 2009). The presence of black bars (or saddles) in all five species may be phylogenetically informative as Merilaita and Kelley (2018) demonstrated that barred color patterns are generally concentrated in a few groups of closely related damselfishes (e.g., Abudefduf , Amphiprion ); this group would be another example. Among these fishes, all have uniserial teeth (Allen, 1975a; Allen and Rajasuriya, 1995; Allen and Adrim, 2000) except for C. annulata , which has biserial teeth ( Smith, 1960; Allen and Randall, 1974, 1981); Chrysiptera tricincta occasionally has irregularly biserial teeth anteriorly (Allen and Randall, 1974). They all share a habitat preference for sand or silt substrates (Allen, 1975a, 1991; Allen and Rajasuriya, 1995; Randall et al., 1997; Allen and Adrim, 2000; Allen et al., 2003; Randall, 2005; Cooper et al., 2009; Lepoint et al., 2016). Parts of the diagnosis for Amblypomacentrus given in Allen (1975a) apply to the three ‘‘ Chrysiptera ’’ (e.g., notch between preorbital and suborbital absent; dorsal spines XIII; preorbital and suborbital naked; snout mostly naked; Peters, 1855; Smith, 1960; Allen and Randall, 1974, 1981; Allen, 1991; Allen and Rajasuriya, 1995). Aside from the variation in tooth rows already mentioned, other deviations from the diagnosis include the extent of preopercular and suborbital serration (preopercle entire in C. tricincta , anterior portion of suborbital often entire in C. kuiteri and C. tricincta ; vs. finely serrated in Amblypomacentrus sensu stricto) and tooth shape (conical in ‘‘ Chrysiptera ’’ vs. incisiform anteriorly in Amblypomacentrus sensu stricto; Smith, 1960; Allen and Randall, 1974, 1981; Allen and Rajasuriya, 1995). Based on the relationships shown herein ( Fig. 1 ), these three species of ‘‘ Chrysiptera ’’ are hereby referred to Amblypomacentrus . Amblypomacentrus is masculine whereas Chrysiptera is feminine so, to match gender, A. annulatus and A. tricinctus are modified accordingly.

Unfortunately, there appear to be no available names for either the herbivorous or Oceanic clades of ‘‘ Chrysiptera .’’ Glyphidodontops and Iredaleichthys , as unneeded replacement names of Chrysiptera with the same type species ( Glyphisodon azureus ), are both objective synonyms of Chrysiptera ( ICZN, 1999: Art. 61.3.3). The type species of Paraglyphidodon is C. oxycephala which is recovered within Chrysiptera sensu stricto ( Fig. 1 ). Further study with more comprehensive taxon sampling is needed to resolve the limits of the different lineages. Eventually, as it is highly unlikely that Chrysiptera sensu lato is monophyletic, new genus-group names will need to be established for the other ‘‘ Chrysiptera .’’

From comments in the literature, some tentative assignments can be made for the species of ‘‘ Chrysiptera ’’ we were unable to examine. Chrysiptera albata and C. caeruleolineata appear to be closely related, based on the following shared characteristics: XIV dorsal spines (vs. XIII in others); smallest ‘‘ Chrysiptera ’’ (, 38 mm SL); deepest occurence of any ‘‘ Chrysiptera ’’ (. 25 m); and preference for sand and rubble habitat over steep outer reefs (Allen and Bailey, 2002; Randall, 2005; Allen and Erdmann, 2012). In the original description, Allen (1973b) likened the color pattern of C. caeruleolineata to that of C. leucopoma . The two species share a neon blue dorsal stripe, for which C. caeruleolineata is named, that is also present in some C. biocellata , C. brownriggii , and C. unimaculata , all species that are closely related to C. leucopoma . Therefore, it is possible that C. albata and C. caeruleolineata are closely related to C. leucopoma and its relatives (herbivorous ‘‘ Chrysiptera ’’). However, they would be the only members of the clade that are not reported to be algal farmers ( Pratchett et al., 2016). Both species also occur at greater depths, below 25 m and extending past 50 m, than the other herbivorous ‘‘ Chrysiptera ’’ (Allen, 1973b, 1975a; Allen and Bailey, 2002). Allen (1975a) thought C. caeruleolineata may warrant separate subgeneric status because of its higher dorsal spine count, predorsal scalation, and uniserial teeth (all shared by C. albata ; Allen and Bailey, 2002). Further investigation is required. We did not include sequences on GenBank labeled as C. caeruleolineata ( FJ459574 – FJ459575 ) for analysis because they originate from the western coast of India in the Arabian Sea, which is outside of its known range (Allen, 1973b, 1975a, 1991). Chrysiptera niger is also likely part of the herbivorous clade because of similarities to C. biocellata , C. glauca , C. leucopoma , and C. unimaculata in appearance, diet, habitat, and meristic counts (Allen, 1975a, 1975c). Although C. niger is not known to practice algal gardening ( Pratchett et al., 2016), its diet does consist primarily of algae (Allen, 1975a, 1975c). Chrysiptera sheila is thought to be most closely related to C. unimaculata , which would make it another herbivorous ‘‘ Chrysiptera ’’ ( Randall, 1994, 1995). DiBattista et al. (2016) appeared to confirm this by finding it sister to C. unimaculata , but their data are not currently available on GenBank. Chrysiptera bleekeri most resembles C. flavipinnis (Allen, 1991, 1997; Allen et al., 2003; Allen and Erdmann, 2012). Based on previous literature describing its overall similarity to C. galba (Allen and Randall, 1974) and C. rapanui (Allen and Randall, 1974; Allen, 1975c), C. notialis is almost certainly an Oceanic ‘‘ Chrysiptera ,’’ a group that includes those species plus C. starcki .

Figures

FIG. 1. The phylogenetic relationships of damselfishes (Teleostei: Pomacentridae): (A) outgroup taxa; (B) subfamilies Microspathodontinae and Glyphisodontinae; (C) subfamily Chrominae; (D) subfamily Pomacentrinae (part I); (E) subfamily Pomacentrinae (part II). The phylogeny is based on the maximum-likelihood topology with the best log likelihood score (ln L ¼ –45,4518.728) recovered from ten independent maximum-likelihood analyses of a data matrix composed of 462 taxa and 6,865 nucleotides. Bootstrap values from 1,000 ultrafast replicates are displayed for each node