Chrominae (sensu Allen, 1975)

Tang, Kevin L., Stiassny, Melanie L. J., Mayden, Richard L. & DeSalle, Robert, 2021, Systematics of Damselfishes, Ichthyology & Herpetology 109 (1), pp. 258-318 : 270-272

Subfamily Chrominae

The subfamily Chrominae is recovered as the sister group of the subfamily Pomacentrinae , a phylogenetic position that corroborates some earlier studies ( Tang, 2001; Jang-Liaw et al., 2002; Quenouille et al., 2004; Tang et al., 2004; Hofmann et al., 2012; Litsios et al., 2012b; Rabosky et al., 2018) but contradicts others (Cooper et al., 2009; Cowman and Bellwood, 2011; Hubert et al., 2011; Litsios et al., 2012a; Betancur-R. et al., 2013a, 2015, 2017; Frédérich et al., 2013; Lobato et al., 2014; DiBattista et al., 2016; Mirande, 2016; Sanciangco et al., 2016; Gaboriau et al., 2018; Delrieu-Trottin et al., 2019). The generic composition of the group has been stable since Cooper et al. (2009) restricted Chrominae to include only Chromis , Dascyllus , and Azurina , a taxonomic change supported by a host of other studies that have found the other putative chromine genera ( Acanthochromis , Altrichthys , and Mecaenichthys ) elsewhere in the pomacentrid tree (e.g., Tang, 2001; Jang-Liaw et al., 2002; Quenouille et al., 2004; Tang et al., 2004; Cowman and Bellwood, 2011; Hofmann et al., 2012; Litsios et al., 2012a, 2012b; Betancur-R. et al., 2013a, 2015, 2017; Frédérich et al., 2013; Rabosky et al., 2013, 2018; Lobato et al., 2014; DiBattista et al., 2016; Mirande, 2016; Sanciangco et al., 2016; Gaboriau et al., 2018; Delrieu-Trottin et al., 2019). The subfamily is dominated by a single genus, Chromis . As the most species-rich genus in the family, Chromis has always been a broad, expansive taxon, though it was generally considered to be a natural assemblage (e.g., Randall and Swerdloff, 1973). However, no study with sufficient taxon sampling has inferred a monophyletic Chromis . It is always rendered non-monophyletic by the placement of Azurina and Dascyllus ( Tang, 2001; Jang-Liaw et al., 2002; Quenouille et al., 2004; Tang et al., 2004; Cooper et al., 2009; Cowman and Bellwood, 2011; Hubert et al., 2011; Hofmann et al., 2012; Litsios et al., 2012a, 2012b; Betancur-R. et al., 2013a, 2015, 2017; Frédérich et al., 2013; Rabosky et al., 2013, 2018; Lobato et al., 2014; DiBattista et al., 2016; Mirande, 2016; Sanciangco et al., 2016; Gaboriau et al., 2018; Delrieu-Trottin et al., 2019).

Based on the extent of taxon sampling herein, it is feasible to address the polyphyly of Chromis . The type species of all genus-group names in the synonymy of Chromis are included in this analysis except for Azurina eupalama , the type of Belochromis , which may be extinct ( Grove and Lavenberg, 1997; Roberts and Hawkins, 1999; Hawkins et al., 2000; Allen et al., 2010c; McCosker and Rosenblatt, 2010) though more extensive surveying is needed for confirmation ( Dulvy and Polunin, 2004; Russell and Craig, 2013). Eighty-one of the 108 currently recognized species of Chromis were examined; Fricke et al. (2020) recognizes 109 species, including C. flavomaculata , which we treat as a synonym of C. notata (see below), following Iwatsubo and Motomura (2013). The results of this study corroborate earlier findings which consistently demonstrated that Chromis , as currently constituted, is broadly polyphyletic. Based on the phylogeny ( Fig. 1 ; Supplemental Fig. 1 ; see Data Accessibility), the putative species of Chromis fall into three disjunct clades. The crown clade includes the type species, Chromis chromis . A second clade is sister to a monophyletic Dascyllus ; this group includes various two-tone species (e.g., C. fieldi , C. iomelas , C. margaritifer ) as well as the miniature species ( C. acares , C. nigrura , C. vanderbilti ). The third clade includes Azurina . The two most obvious solutions for the polyphyly of Chromis are: 1) place Azurina and Dascyllus in the synonymy of Chromis ; or 2) assign those species currently classified as Chromis , but not most closely related to Chromis chromis , to different genera. The first choice would result in the reclassification of two species of Azurina and 11 species of Dascyllus into an already sprawling Chromis , which would cause at least one instance of secondary homonymy ( Chromis flavicauda vs. Dascyllus flavicaudus ; ICZN, 1999: Art. 57.3.1). The second choice would retain both Azurina and Dascyllus , and break up Chromis into multiple genera. We have chosen the latter option.

Because the crown group includes the type species Chromis chromis , it remains Chromis . The clade sister to Dascyllus includes C. vanderbilti , the type species of Pycnochromis . Therefore, we hereby refer all species of Chromis in that clade (abrupta, acares , alleni , amboinensis , atripes , caudalis, delta, dimidiata, fatuhivae , fieldi , hanui , howsoni , iomelas , leucura, margaritifer , nigrura , ovatiformis , pacifica , retrofasciata, and vanderbilti ) to Pycnochromis . The genus is masculine so several specific epithets must change to agree in gender (e.g., abruptus , dimidiatus , retrofasciatus). The species name pacifica is treated as a noun in apposition (Allen and Erdmann, 2020: 109), so the suffix does not change to match the masculine gender of Pycnochromis . This usage of Pycnochromis expands the original limits of the genus, initially established for small, elongate species typified by C. vanderbilti , to absorb a grouping equivalent to Allen’s (1975a: 38) margaritifer complex [¼ Chromis amboinensis complex sensu Allen and Erdmann, 2020 ], which was characterized by the presence of XII dorsal spines, exposed suborbital [¼ infraorbital] margin, and bifurcate (occasionally trifurcate) filaments at the margin of each caudal-fin lobe. Those species of Chromis most closely related to Azurina hirundo ( C. atrilobata , C. brevirostris , C. cyanea , C. elerae , C. lepidolepis , and C. multilineata ) are referred to Azurina . Azurina is feminine, so no name changes are necessary for gender agreement. Following this reorganization within the Chrominae , the subfamily is divided into four genera: Azurina sensu novum , Chromis sensu stricto, Dascyllus , and Pycnochromis sensu novum .

The total number of procurrent rays on each edge of the caudal peduncle is variable across the Pomacentridae , with species of Chromis (5–6) and Dascyllus (5) having fewer than other genera in the family ( Randall et al., 1981). Without a comprehensive survey of this character, it is impossible to know if the number of procurrent caudal rays is phylogenetically informative at this level. However, the presence and numbers of a subset of these rays, the protruding spiniform rays (occasionally called caudal spinules; e.g., Randall et al., 1981; Shao et al., 1985; Yamakawa and Randall, 1989), have played a role in the classification of the subfamily (e.g., Allen, 1975a, 1999a; Koh et al., 1997; Kavanagh et al., 2000) and within Chromis ( Randall and Swerdloff, 1973; Allen, 1975a; Greenfield and Woods, 1980). Since its prominent role in the classification proposed by Allen (1975a), the presence of spiniform procurrent rays has been regarded as a diagnostic character for the Chrominae . However, it is now apparent that some non-chromine taxa also possess this feature. Acanthochromis , Altrichthys , and Mecaenichthys , three genera previously classified in Chrominae , and Parma , a genus not historically associated with Chrominae , all possess this type of ray (Allen, 1975a, 1991; Hensley, 1986). Hensley (1986: 861) reported the presence of protruding procurrent caudal-fin rays in Parma , noting its significance as a diagnostic feature for the subfamily Chrominae (sensu Allen, 1975a) . Cooper et al. (2009) discouraged the use of this character for taxonomic purposes because of its appearance in species outside of Chrominae sensu stricto. Cooper and Santini (2016) considered it unreliable as a diagnostic character. Although their presence does not characterize Chrominae as originally constituted, the number of exposed spiniform rays appears to have phylogenetic signal within the subfamily. The character state varies between 0 and 3 rays across the Chrominae ; this condition has not been reviewed for the entire subfamily and its state is not available for all species so data were compiled from the following: Emery (1968); Greenfield and Hensley (1970); Randall and Swerdloff (1973); Randall and McCarthy (1988); Allen (1976, 2018); Randall and Allen (1977, 1982); Bruner and Arnam (1979); Greenfield and Woods (1980); Smith-Vaniz and Emery (1980); Allen and Randall (1981, 1985, 2004a); Randall et al. (1981); Emery and Smith-Vaniz (1982); Shao et al. (1985); Edwards (1986); Randall (1988a, 1988b, 1994, 2001); Randall and Follett (1989); Yamakawa and Randall (1989); Randall and McCosker (1992); Moura (1995); Randall and Randall (2001); Lecchini and Williams (2004); Allen and Erdmann (2005, 2008a, 2009a, 2014); McEachran and Fechhelm (2005); Senou and Kudo (2007); Pyle et al. (2008); Quéro et al. (2010); Aguilar-Medrano (2013); Iwatsubo and Motomura (2013); Randall and DiBattista (2013); Motomura et al. (2017); Yoshigou (2017); Arango et al. (2019); Tea et al. (2019); Allen and Erdmann (2020); Shepherd et al. (2020). The presence of two spiniform rays is widespread across the subfamily, whereas the presence of three spiniform rays appears mostly confined to the subgenus Chromis (see below) within Chromis sensu stricto. However, three spiniform rays are also observed elsewhere (e.g., C. atripectoralis , C. flavaxilla ; Randall et al., 1981; Randall, 1994).

The majority of the species within the subfamily possess XII dorsal-fin spines. Except for A. brevirostris (XIII) and A. eupalama (XIII–XIV), species of Azurina sensu lato have XII dorsal spines (Allen, 1991; Pyle et al., 2008). All species of Dascyllus exhibit XII spines (Allen, 1991). All species of Pycnochromis display XII spines, at least modally (sometimes XI in P. howsoni , sometimes XIII in P. abruptus , P. acares , P. alleni , P. ovatiformis ; Allen, 1991; Randall and McCosker, 1992; Randall, 2001; Randall and DiBattista, 2013; Allen and Erdmann, 2014). The species of Chromis sensu stricto show the most variation, ranging from XII to XV. The species of the subgenus Hoplochromis (see below) modally have XII ( Randall et al., 1981; Allen, 1991; Randall, 1994). The remaining members of Chromis sensu stricto generally have XIII or more dorsal spines ( Griffin, 1923; Allen, 1991, 2018; Randall and McCosker, 1992; Moura, 1995; Randall, 2001; Allen and Randall, 2004a; Lecchini and Williams, 2004; Allen and Erdmann, 2005, 2008a, 2009a; Senou and Kudo, 2007; Pyle et al., 2008; Quéro et al., 2010; Iwatsubo and Motomura, 2013, 2018; Motomura et al., 2017; Arango et al., 2019; Tea et al., 2019; Shepherd et al., 2020).

Other morphological characters may be phylogenetically informative, but a thorough review of these characters will be necessary to assay their phylogenetic utility. The presence of the ceratomandibular ligament has been interpreted as a synapomorphy of the family as a whole ( Stiassny, 1981; Frédérich et al., 2014; Olivier et al., 2016) and there is considerable variation in the condition within the subfamily Chrominae , but the ligament has been either lost and/or regained independently multiple times among chromines ( Frédérich et al., 2014: fig. 2). As a result, the phylogenetic significance of its loss is difficult to determine. Tooth shape is a trait with a long history in damselfish taxonomy, where putative chromines were diagnosed on the basis of conical teeth (e.g., Bleeker, 1877; Whitley, 1929; Aoyagi, 1941; Smith, 1949; Norman, 1957; Woods and Schultz, 1960; Marshall, 1964; Masuda et al., 1975). However, the condition of the teeth is highly variable within the subfamily and across the family. Several non-chromine taxa also possess similarly shaped teeth (e.g., Acanthochromis , Amphiprion , Lepidozygus ; Allen, 1972, 1975a, 1991; Emery, 1980).

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