Pomacentrus, Lacepède, 1802

Tang, Kevin L., Stiassny, Melanie L. J., Mayden, Richard L. & DeSalle, Robert, 2021, Systematics of Damselfishes, Ichthyology & Herpetology 109 (1), pp. 258-318 : 296-298

Pomacentrus .

— The members of Pomacentrus are widely distributed across the tropical Indo-West Pacific, with the majority concentrated in the western and central Pacific (Allen and Randall, 2004b, 2005; Allen and Erdmann, 2009b; Allen et al., 2011, 2017b, 2018b). After the restructuring herein of Chromis sensu lato (108 species), which significantly reduced the size of Chromis sensu stricto (76 species), Pomacentrus is now the largest genus in the family (81 species; Fricke et al., 2020). Its high species diversity has been attributed to an increased rate of diversification (Cowman and Bellwood, 2011; Lobato et al., 2014). Of the 81 species currently recognized in the genus, 54 were examined for this study plus an additional undescribed species ( Pomacentrus cf. microspilus ). Monophyly of the genus Pomacentrus received strong branch support (100% bootstrap), which agrees with most prior studies ( Jang-Liaw et al., 2002; Quenouille et al., 2004; Tang et al., 2004; Bernardi, 2011; Hubert et al., 2011; Hofmann et al., 2012; Litsios et al., 2012a; Rabosky et al., 2013, 2018; Lobato et al., 2014; Mirande, 2016; Gaboriau et al., 2018; Stieb et al., 2017; Delrieu-Trottin et al., 2019). Where there was disagreement, it mainly came from analyses that relied on Cooper et al. (2009) for data representing Altrichthys curatus (e.g., Cowman and Bellwood, 2011; Litsios et al., 2012b; Frédérich et al., 2013; DiBattista et al., 2016). As discussed above, there is convincing evidence that Cooper et al. (2009) did not infer a monophyletic Pomacentrus because their sequences for Altrichthys were erroneous (Bernardi, 2011). Aside from that anomalous result and the misidentified ‘‘ Pomacentrus agassizii ’’ (see above), there is robust support for the monophyly of Pomacentrus .

There are relatively few genus-group names currently in the synonymy of Pomacentrus . The type species of Parapomacentrus ( Pomacentrus polynema ) is currently considered a synonym of Pomacentrus pavo , the type species of Pomacentrus . Pseudopomacentrus was originally erected as a subgenus (type species: P. littoralis ). Allen (1975a: 43) also established Lepidopomacentrus as a subgenus (type species: P. lepidogenys ) and provided a key for the subgenera of Pomacentrus that he recognized ( Lepidopomacentrus , Pomacentrus , and Pseudopomacentrus ). An important character used to differentiate Lepidopomacentrus was the presence of scales on the preorbital and suborbital. However, other species with similar conditions (e.g., P. littoralis , P. philippinus ) were referred to Pseudopomacentrus (Allen, 1975a) . Subsequently, more species of Pomacentrus have been reported with such scales (e.g., P. aquilus , P. arabicus , P. cuneatus , P. komodoensis ; Allen and Randall, 1981; Allen, 1991, 1999b). Pomacentrus callainus was originally considered a color variant of P. lepidogenys ( Randall, 2002) , and they are sister species in our phylogeny ( Fig. 1 ), so it is not surprising they share scaled infraorbitals. Others with this feature are members of the Pomacentrus philippinus complex, for which it is diagnostic: P. albiaxillaris , P. flavoaxillaris , P. magniseptus (variable, usually absent), and P. nigriradiatus (Allen et al., 2017b) . Therefore it would be expected that they also share that trait with the namesake of the complex. Pomacentrus yoshii , which Allen and Randall (2004b) regarded as closely related to P. philippinus but was not included in the P. philippinus complex (Allen et al., 2017b, 2017c), also possesses scales on the infraorbitals. Aside from a brief mention in Allen (2001), the subgeneric framework has gone unused in his subsequent works on Pomacentrus (e.g., Allen and Randall, 1981, 2004b, 2005; Allen, 1991, 1992, 1993, 1995, 1999b, 2002, 2004; Allen and Wright, 2003; Allen and Erdmann, 2009b; Allen et al., 2011, 2017b, 2017c, 2018b; Allen and Drew, 2012). The relationships seen in this study demonstrate that it would be difficult to make use of the existing subgenera without substantial revisions. Based on the location of P. lepidogenys relative to P. littoralis (type species of Pseudopomacentrus ), recognition of Lepidopomacentrus and Pseudopomacentrus as subgenera sensu Allen (1975a) would leave several Pomacentrus clades not included in either. Placing Lepidopomacentrus in the synonymy of Pseudopomacentrus , thereby dividing Pomacentrus into two broad subgenera ( Pomacentrus for P. pavo and its allies; Pseudopomacentrus for the bulk of Pomacentrus ), would resolve that problem but P. xanthosternus , as the sister group of all other Pomacentrus , would still require a subgeneric name and there are no available genus-group names based on that species ( Fricke et al., 2020).

There are three distinct lineages within Pomacentrus . As stated above, P. xanthosternus is the sister species of all other Pomacentrus examined. Pomacentrus xanthosternus has not been the subject of much study but, in its original description, Allen (1991: 233) remarked that the species is ‘‘[c]learly separable from other Pomacentrus by the combination of colour pattern, a relatively low (16) lateral-line count and 23–24 gill rakers.’’ The remaining species are divided into two groups. The first includes the type species, P. pavo , and its allies. These fishes, except for P. caeruleopunctatus (Allen, 2002) , are generally more elongate than other Pomacentrus (body depth usually 2.3 in SL; Allen, 1991; Liu et al., 2013). Allen (1975a: 202) noted that brightly colored, elongate species (e.g., P. coelestis , P. pavo ) are midwater zooplankton specialists, in contrast to other Pomacentrus spp. , which are generalist omnivores. Species of this group exhibit a similar body form as other midwater damselfishes that forage in the water column (e.g., Neopomacentrus , Pomachromis ), where they capture individual prey items via plankton picking (Allen and Emery, 1973; Davis and Birdsong, 1973; Emery, 1983). Hubert et al. (2012: table S3) detected possible cryptic diversity in P. pavo , which they characterized as geographic monophyly with deep divergence (their ‘‘Pattern 2’’) between individuals of P. pavo from French Polynesia compared to those from Madagascar. Hubert et al. (2017: fig. 3, tables S3, S4) showed similar results, finding reciprocal monophyly between lineages from the Indian and Pacific Oceans (their ‘‘Pattern II.1’’). Allen (1991) reported coloration differences between the two populations, where ‘‘[w]estern Indian Ocean specimens frequently have pronounced black margins on the dorsal and anal fins.’’ Allen and Randall (2004b) noted that it has the widest range of any Pomacentrus , extending from the western Indian Ocean (east Africa) to the central Pacific (Tuamotu Islands), in a genus whose species are otherwise more geographically restricted and seemingly widespread species are often complexes of cryptic species (Allen et al., 2017b). As the type species of Pomacentrus , any changes to its species limits could have nomenclatural implications. In such a scenario, the Indo-Australian lineage (type locality: East Indies; Bloch, 1787) would retain the name P. pavo . No apparent available names exist for the western Indian Ocean population, if it does indeed represent hidden diversity. Of the names in the synonymy of P. pavo (Allen, 1991; Fricke et al., 2020), all appear to originate from regions outside of the western Indian Ocean.

The clade with P. pavo can be further subdivided into two lineages: P. pavo plus its sister species, P. leptus , in one and the neon damsels in the other. The latter group has been called different names by various authors: ‘‘blue damsel’’ complex (Allen, 1991: 232), P. coelestis complex ( Liu et al., 2013), Pomacentrus coelestis species complex ( Sorenson et al., 2014), Pomacentrus coelestis complex ( Getlekha et al., 2018). This set of species currently comprises P. alleni , P. auriventris , P. caeruleopunctatus , P. caeruleus , P. coelestis , P. micronesicus , and P. similis . They are slender planktivores with brilliant blue coloration, sometimes accompanied by varying amounts of bright yellow markings. Their similarities have been discussed before (e.g., Allen, 1991, 2002; Myers, 1999; Liu et al., 2012, 2013; Sorenson et al., 2014). Getlekha et al. (2018) found that members of this clade displayed the conserved karyotype (2n ¼ 48; NF ¼ 48) compared to other Pomacentrus , which usually have much higher fundamental numbers (76; Ojima, 1983; Klinkhardt et al., 1995; Molina and Galetti, 2004b; Arai, 2011). They proposed a potential synapomorphy for this group: ‘‘organization of ribosomal genes in a syntenic, but non-colocalized array’’ on the long arm of chromosome 5. Although their sampling was limited to only two species ( P. auriventris and P. similis ), both clades seen in Sorenson et al. (2014) were represented, one from each ocean basin. Our data matrix included all species except P. caeruleopunctatus , for the reasons discussed below. The phylogenetic relationships we recovered within this complex are compatible with those previously reported ( Liu et al., 2013: fig. 4; Sorenson et al., 2014: fig. 2). The species fall into two geographically discrete clades: one inhabiting the Indian Ocean ( P. alleni , P. caeruleus , and P. similis ) and the other inhabiting the Pacific Ocean ( P. auriventris , P. coelestis , and P. micronesicus ). In the Indian Ocean clade, P. similis is sister to P. alleni þ P. caeruleus ; in the Pacific clade, P. micronesicus is sister to P. auriventris þ P. coelestis . With denser intraspecific sampling, Sorenson et al. (2014) found possible cryptic diversity in P. micronesicus (corroborating Liu et al., 2012), P. auriventris nested within P. coelestis , and P. caeruleopunctatus nested within P. caeruleus . The last result caused Sorenson et al. (2014) to raise questions about whether P. caeruleopunctatus is distinct from P. caeruleus . However, that outcome was likely due to an identification error because the voucher specimen of the only P. caeruleopunctatus in their phylogeny ( Sorenson et al., 2014: fig. 2; ‘‘cap_mad77347’’) appears to have been misidentified at the time of their study. Upon further examination, the fishes in SAIAB 77347 (KU T6913), originally labeled as P. caeruleopunctatus , have all been reidentified as P. caeruleus because they display only one horizontally elongate mark on the scales of the posterior body (O. Gon, pers. comm.). That character differentiates P. caeruleus from P. caeruleopunctatus , which usually has 2–3 such marks on each scale (Allen, 2002). This affects the following GenBank records: JQ707052 , JQ707087 , JQ707119 , JQ707154 , JQ707181 , JQ707209 , JQ707245 , JQ707280 ( Frédérich et al., 2013: table S1), KM198744 , KM198842 ( Sorenson et al., 2014: 2505). The only novel record presently available on BOLD (UKFBJ948-08) also originated from SAIAB 77347. The lone sequence attributed to this species that is not derived from SAIAB 77347 was also published in Sorenson et al. (2014). They sequenced cyt b ( KM198771 ) from a different specimen (SAIAB 80854) that did not appear in their phylogeny. That fish has also been reidentified as P. caeruleus for the same diagnostic reasons given above (O. Gon, pers. comm.). As a result, there are no confirmed sequences of P. caeruleopunctatus currently available. Its relationships and status remain unresolved.

The remainder of Pomacentrus falls into a single large clade. Its basal group is composed of western Indian Ocean species that primarily have XIV dorsal-fin spines. Species of Pomacentrus typically display XIII spines (Allen, 1991; Allen and Wright, 2003). There are 21 species that possess a modal count of XIV dorsal spines: P. aquilus , P. arabicus , P. armillatus , P. atriaxillaris , P. australis , P. baenschi , P. bangladeshius , P. bellipictus , P. fakfakensis , P. indicus , P. milleri , P. opisthostigma , P. pikei , P. polyspinus , P. proteus , P. reidi , P. rodriguesensis , P. stigma , P. sulfureus , P. trichrourus , and P. vatosoa (Allen, 1991, 1993, 2002; Allen and Wright, 2003; Allen and Erdmann, 2009b; Allen et al., 2018b; Frable and Tea, 2019; Habib et al., 2020). Allen and Wright (2003) observed that species with XIV dorsal spines are concentrated in the Indian Ocean, particularly in the western Indian Ocean, where almost half of them are found ( P. aquilus , P. arabicus , P. atriaxillaris , P. baenschi , P. indicus , P. pikei , P. rodriguesensis , P. sulfureus , P. trichrourus , and P. vatosoa ; Allen, 1991, 1993, 2002; Allen and Wright, 2003; Frable and Tea, 2019). They speculated that ‘‘many of these species, particularly from the western Indian Ocean, appear to be closely related on the basis of general morphology.’’ The five XIV-spined species from the western Indian Ocean included in our phylogeny ( P. aquilus , P. baenschi , P. sulfureus , P. trichrourus , and P. vatosoa ) did form a monophyletic group that also included two XIII-spined species, P. albicaudatus , which is endemic to the Red Sea, and P. trilineatus , which also occurs in the western Indian Ocean. Despite having fewer dorsal spines, P. trilineatus has been associated with P. baenschi (Allen, 1991: 226) , which we found as its sister species. Frable and Tea (2019) resolved a similar clade consisting of P. baenschi , P. trichrourus , P. trilineatus , and P. vatosoa ; they did not examine P. albicaudatus or P. aquilus and recovered P. sulfureus apart from the others. Improved taxon sampling will be necessary to ascertain if all Pomacentrus with XIV spines from the region are closely related. GenBank sequences reported as Pomacentrus arabicus from Madagascar by Hubert et al. (2011) were not included; they appear extralimital because that species is endemic to the Gulf of Oman (Allen, 1991; Randall, 1995; Fricke et al., 2018). Those sequences of ‘‘ P. arabicus ’’ were identified as P. trilineatus by the BOLD Identification Engine and GenBank BLAST. This applies to the following GenBank records: JF435099 , JF457583 , JF458212 . True P. arabicus is probably closely related to P. aquilus on the basis of their shared dark coloration, western Indian Ocean distribution, and possession of XIV dorsal spines (Allen, 1991: 223).

The genus contains several species of territorial herbivores that cultivate algal mats (i.e., gardeners). Information on dietary habits is incomplete but they include at least P. adelus , P. aquilus , P. bankanensis , P. burroughi, P. chrysurus , P. grammorhynchus , P. tripunctatus , P. vaiuli , and P. wardi (Ceccarelli, 2007; Hoey and Bellwood, 2010; Frédérich et al., 2013: fig. 3; Hata and Ceccarelli, 2016; Pratchett et al., 2016). Allen (1975a, 1997) observed that herbivorous species (e.g., P. burroughi , P. wardi ) tend to be drab, whereas planktivorous species (e.g., P. alexanderae , P. popei ) tend to be colorful. One clade in particular contains a cluster of several algal farmers: P. bankanensis , P. burroughi , P. grammorhynchus , P. vaiuli , and P. wardi . However, other such species with similar diets are dispersed across the genus.

Recently, Allen et al. (2017b, 2017c) circumscribed a ‘‘ Pomacentrus philippinus complex.’’ In addition to its namesake species, the species group also includes P. albiaxillaris , P. flavioculus , P. flavoaxillaris , P. imitator , P. magniseptus , and P. nigriradiatus . They share several characteristic features: pale caudal fins (clear, orange, whitish, or yellow) with matching coloration for the posterior sections of the anal and soft dorsal fins; absence of dorsal-fin ocellus in juveniles; short filamentous extensions of the caudal-fin lobes; presence of infraorbital scales (usually absent in P. flavioculus and P. imitator ); network pattern formed by dark scale margins; and prominent black spot at pectoral-fin base (Allen et al., 2017b, 2017c). Allen et al. (2017c) found that P. imitator and P. magniseptus share mtDNA sequences, but commented that they are easily separated because of their allopatric distributions and diagnostic differences in coloration. However, our results did not show a monophyletic philippinus complex, with P. flavioculus apart from the rest of the species complex, which is monophyletic. The COI sequences of Pomacentrus philippinus ( KY463238 , KY463239 , KY463240 ) from Allen et al. (2017b) are more similar to Chromis than Pomacentrus , showing greater than 99% identity with published C. alpha ( JF434867 ) and C. degruyi ( EU358588 ) data in BLAST and BOLD searches. However, the 16S sequences ( MF828512 , MF828513 , MF828514 ) from Allen et al. (2017c) are most similar to other species from the Pomacentrus philippinus complex. The cause of this discrepancy is unclear. Although voucher information is not available, the corresponding loci appear to have been collected from the same samples, based on GenBank record information. The specimens were collected at Palawan, Philippines (Allen et al., 2017b: fig. 17; 2017c: fig. 5). We only analyzed 16S ( MF828512 ) for the representative of P. philippinus in our phylogeny ( Fig. 1 ; Supplemental Table 1; see Data Accessibility).

Outside of the various family-wide phylogenies, there have been few studies focused on relationships within Pomacentrus ( Liu et al., 2013; Sorenson et al., 2014; Allen et al., 2017b, 2017c; Frable and Tea, 2019; Habib et al., 2020). Many of the relationships inferred in our phylogeny corroborated earlier hypotheses. We resolved a sister-group relationship between P. alexanderae and P. nigromanus that was suggested by Allen (1991). We recovered a clade with 100% bootstrap support that included P. amboinensis , P. maafu , and P. moluccensis ( Randall et al., 1997; Allen and Drew, 2012). Cooper et al. (2009) recovered P. albicaudatus sister to an equivalent group ( P. amboinensis þ P. moluccensis ), but their specimen (FMNH 126547) was collected in the Philippines, which is well outside its native range as a Red Sea endemic (Allen and Randall, 1981; Allen, 1991; DiBattista et al., 2016; Golani and Fricke, 2018; Atta et al., 2019). This affects the following GenBank records: FJ616364 , FJ616472 , FJ616578 , FJ616690 , FJ616803 , FJ616911 . Our analysis resolved a specimen identified as P. albicaudatus from the Red Sea ( MN560894 ; Atta et al., 2019) as sister to P. sulfureus and part of a western Indian Ocean clade whose members predominantly have XIV dorsal spines (see above). We recovered a clade that includes P. armillatus , P. bankanensis , and P. vaiuli , which have been linked in previous works (Allen, 1993; Randall et al., 1997; Myers, 1999; Randall, 2005). The P. aurifrons – P. smithi sister pairing (100% bootstrap) has also been posited in the literature before (Allen, 2004; Randall, 2005; Allen and Erdmann, 2012).

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