Systematics of Damselfishes Author Tang, Kevin L. Author Stiassny, Melanie L. J. Author Mayden, Richard L. Author DeSalle, Robert text Ichthyology & Herpetology 2021 2021-05-05 109 1 258 318 http://dx.doi.org/10.1643/i2020105 journal article 53279 10.1643/i2020105 cf572f6b-8843-4383-85ce-ac9ea8515e87 2766-1520 7846738 Subfamily Glyphisodontinae The species of Abudefduf , the sole genus in this subfamily, have a widespread circumtropical distribution. We included all 21 currently recognized species ( Wibowo et al., 2018 ; Fricke et al., 2020 ), but there is compelling evidence of undescribed diversity within Abudefduf vaigiensis ( Quenouille et al., 2011 ; Bertrand et al., 2017; Campbell et al., 2018; Wibowo et al., 2018 ) which we did not include. All species except A. sparoides have a distinctive color pattern of alternating light and dark vertical bars ( Hensley, 1978 ), giving the group its common name, ‘‘sergeants.’’ They are united by their deep bodies and possession of ‘‘uniserial teeth with compressed tips and bicuspid or entire margins (in adults)’’ and ‘‘13 dorsal spines (rarely 12 or 14)’’ ( Hensley and Allen, 1977 ). The monophyly of Abudefduf (with the exception of Similiparma lurida ) has not been in doubt since Allen (1975a) greatly restricted the genus to a taxon equivalent to the subgenus Glyphidodon [ ¼ Glyphisodon ] sensu Bleeker (1877) . According to Getlekha et al. (2016a) , the genus exhibits ‘‘chromosomal conservatism,’’ based on the limited variation in cytogenetic characteristics (e.g., conserved chromosome and fundamental numbers, karyotype structure) among its species. They suggested that this lack of divergence contributed to the hybridization observed between A. abdominalis and A. vaigiensis ( Maruska and Peyton, 2007 ; Coleman et al., 2014), because cytogenetic differences (e.g., pericentric inversions) can serve as strong post-zygotic barriers to viable hybrids. Despite the degree of chromosomal similarity seen in Abudefduf , Getlekha et al. (2016a : fig. 5) did report a potential cytogenetic synapomorphy within the genus. In their investigation of pomacentrid egg and larval morphology, Muñoz-Cordovez et al. (2019) observed that larvae of Abudefduf concentrate pigmentation in the pre-anal segment of the body, whereas pigment is primarily postanal in the other subfamilies. Our phylogeny ( Fig. 1 ; Supplemental Fig. 1 ; see Data Accessibility) resolves a monophyletic Abudefduf sensu stricto , excluding ‘‘ Abudefduf ’’ luridus [ ¼ Similiparma lurida ], which Cooper et al. (2014) referred to the microspathodontine genus, Similiparma . We follow Cooper and Santini (2016) in recognizing the subfamily Glyphisodontinae for the species of Abudefduf . The subfamily is sister to a clade comprising the subfamilies Chrominae and Pomacentrinae . This placement of Abudefduf is supported by some studies ( Quenouille et al., 2004 ; Hofmann et al., 2012 ; Litsios et al., 2012b ; Stieb et al., 2017 : fig. 1; Rabosky et al., 2018 ) but disagrees with those that have located Glyphisodontinae as the sister group of Chrominae ( Hubert et al., 2011 ; Stieb et al., 2017 : fig. 2), Microspathodontinae (Delrieu-Trottin et al., 2019), or Pomacentrinae (Cooper et al., 2009; Cowman and Bellwood, 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 ). Regardless of its exact position, the genus is consistently resolved apart from the other subfamilies, supporting its treatment as a distinct subfamily by Cooper and Santini (2016). Karyotype data ( Molina and Galetti, 2004a ; Molina, 2007 ) appear to corroborate this conclusion by finding substantial divergence between Abudefduf and members of Pomacentrinae . The genus can be divided into three monophyletic groups that correspond to the genus-group names Euschistodus ( type species: A. declivifrons ), Abudefduf ( type species: A. sordidus ), and Glyphisodon ( type species: A. saxatilis ). We treat these as subgenera in the following discussion of relationships within Abudefduf . Thus, Abudefduf ( Euschistodus ) is sister to a clade of Abudefduf ( Abudefduf ) þ Abudefduf ( Glyphisodon ) . We found strong bootstrap support for each clade and that pattern of relationships (100% bootstrap at each node; Fig. 1 ). These relationships are consistent with earlier studies ( Quenouille et al., 2004 ; Cowman and Bellwood, 2011; Litsios et al., 2012a , 2012b ; Frédérich et al., 2013 ; Rabosky et al., 2013 , 2018 ; DiBattista et al., 2016; Bertrand et al., 2017; Campbell et al., 2018; Gaboriau et al., 2018 ; Delrieu-Trottin et al., 2019). Aguilar-Medrano et al. (2011) identified two different trophic types in the genus: one with an inferior mouth associated with benthic prey; the other with a superior mouth associated with zooplanktivory. The ancestral condition of the genus, as seen in Abudefduf ( Abudefduf ) and Abudefduf ( Euschistodus ) , appears to be characterized by the following traits ( Hensley, 1978 ; Aguilar-Medrano and Barber, 2016; Campbell et al., 2018): dark bars usually distinctly wider than or at least equal in width to light interspaces, generalist diet (algae, benthic invertebrates, zooplankton), solitary or in small aggregations, preference for shallow surf zones (group a of Aguilar-Medrano and Barber, 2016). The species-rich crown group, Abudefduf ( Glyphisodon ) , is characterized by the following: thin dark bars distinctly narrower than light interspaces (barring pattern lost in A. sparoides ), specialist diet (zooplankton), in large aggregations, preference for reefs, occurrence in water column (group b of Aguilar-Medrano and Barber, 2016). Group a is paraphyletic relative to group b . Campbell et al. (2018) characterized these as benthivores (group a ) versus planktivores (group b ), with one species, A. notatus , described as ‘‘in transition from benthivory to planktivory.’’ The New World night sergeants (subgenus Euschistodus ) are composed of A. concolor , A. declivifrons , and A. taurus . This benthivorous group corresponds to ‘‘Clade A’’ or the ‘‘ taurus clade’’ of Campbell et al. (2018). These species form a clade that is sister to the remaining Abudefduf . Other studies have corroborated a monophyletic Euschistodus sister to the rest of the genus (e.g., Quenouille et al., 2004 ; Cowman and Bellwood, 2011; Litsios et al., 2012a , 2012b ; Frédérich et al., 2013 ; Rabosky et al., 2013 , 2018 ; DiBattista et al., 2016; Campbell et al., 2018; Gaboriau et al., 2018 ; Delrieu-Trottin et al., 2019). Lessios et al. (1995) examined their relationships using a mix of isozymes, DNA sequences, and morphological data. They recognized A. declivifrons , previously considered a subspecies of A. concolor (e.g., Allen, 1991: 234), as a distinct species sister to A. concolor þ A. taurus . Hensley (1978) identified a potential synapomorphy for the trans-isthmus geminate pair of A. concolor and A. taurus : suborbitals adnate (vs. suborbitals free from cheek in A. declivifrons ). Campbell et al. (2018) reported possible cryptic diversity within A. taurus , with a divide between the eastern and western Atlantic populations. There does not appear to be an available name for the eastern Atlantic lineage, if it is a separate species. Species of Euschistodus tend to have fewer anal rays (usually ten) than other species of Abudefduf , which usually have 11 or more, though A. saxatilis and A. troschelii occasionally have ten ( Hensley, 1978 ; Allen, 1991; Allen and Robertson, 1994; Lessios et al., 1995 ; Robertson and Allen, 2015 ). The three species of the subgenus Abudefduf ( A. notatus , A. septemfasciatus , and A. sordidus ) have been consistently recovered as a monophyletic group ( Quenouille et al., 2004 ; Cooper et al., 2009; Cowman and Bellwood, 2011; Litsios et al., 2012a , 2012b ; Frédérich et al., 2013 ; Rabosky et al., 2013 , 2018 ; Coleman et al., 2014; Lobato et al., 2014 ; DiBattista et al., 2016; Mirande, 2016 ; Vella et al., 2016 ; Bertrand et al., 2017; Campbell et al., 2018; Gaboriau et al., 2018 ; Delrieu-Trottin et al., 2019). Campbell et al. (2018) identified this group as ‘‘Clade B’’ or the ‘‘ sordidus clade,’’ and they classified its species as benthivorous, except for A. notatus which was considered to be ‘‘in transition to planktivory.’’ Hensley (1978) noted that A. septemfasciatus and A. sordidus are the only species of Abudefduf with a conspicuous black spot on the dorsal surface of the caudal peduncle, which could be potentially informative; in A. septemfasciatus , the spot is only present in juveniles. Frédérich et al. (2014) reported another character shared by these two species: modified ceratomandibular ligament fused to geniohyoideus muscle. The subgenus Glyphisodon contains the majority of species of Abudefduf . It is equivalent to ‘‘group b ’’ of Aguilar-Medrano and Barber (2016) and ‘‘Clade C’’ or the ‘‘ saxatilis clade’’ of Campbell et al. (2018). This group within Abudefduf has evolved to become planktivorous, a shift accompanied by a series of changes documented in Aguilar-Medrano and Barber (2016). Based on the distribution of the ceratomandibular ligament ( Frédérich et al., 2014 ), loss of the ligament may be a synapomorphy for Glyphisodon . Within Glyphisodon , A . bengalensis is the only species Frédérich et al. (2014 : fig. 2) classified as a benthic feeder and the only one reported to possess the ligament. Frédérich et al. (2014) concluded that loss of the ligament was associated with zooplanktivory. Our phylogeny shows a clade that includes A. abdominalis , A. conformis , A. hoefleri , A. lorenzi , A. saxatilis , A. sexfasciatus , A. troschelii , and A. vaigiensis . Five of these species ( A. abdominalis , A. conformis , A. saxatilis , A. troschelii , and A. vaigiensis ) have been grouped together as a species complex by earlier workers ( Randall and Earle, 1999 ; Randall, 2005). The three species distributed in the Atlantic and eastern Pacific ( A. hoefleri , A. saxatilis , and A. troschelii ) are recovered as a clade, which corroborates what has been reported before (Cowman and Bellwood, 2011; Litsios et al., 2012a , 2012b ; Frédérich et al., 2013 ; Vella et al., 2016 ; Campbell et al., 2018; Gaboriau et al., 2018 ). However, A. saxatilis and A. troschelii do not form a trans-ishthmian geminate pair as previously suggested in the literature (e.g., Allen, 1976; Gorman and Kim, 1977 ; Vawter et al., 1980 ; Foster, 1987 ; Bermingham et al., 1997; Robertson and Collin, 2015 ) and shown by other phylogenies (DiBattista et al., 2016; Vella et al., 2016 ; Rabosky et al., 2018 ). Instead, the two Atlantic species ( A. saxatilis and A. hoefleri ) are resolved together in a clade, with A. troschelii as its sister taxon, a relationship which agrees with Campbell et al. (2018). They found A. hoefleri grouped with the eastern population of A. saxatilis , rendering A. saxatilis paraphyletic. Other phylogenies have resolved an A. hoefleri þ A. troschelii sister pairing instead (Cowman and Bellwood, 2011; Litsios et al., 2012a , 2012b ; Frédérich et al., 2013 ; Rabosky et al., 2013 ; Gaboriau et al., 2018 ; Delrieu-Trottin et al., 2019). Bertrand et al. (2017) showed that Abudefduf vaigiensis , as currently constituted, is likely polyphyletic, encompassing up to four disjunct lineages. The non-monophyly of A. vaigiensis was first suggested by Bermingham et al. (1997), who recovered two separate lineages: one widespread across the Indo-Pacific and another confined to the western Pacific. Quenouille et al. (2011 : fig. 2b) also showed a polyphyletic A. vaigiensis . Bertrand et al.’s (2017) lineage A, the most abundant of the four, is widespread in the Indo-West Pacific and nested within a paraphyletic A. sexfasciatus , something that was foreshadowed by other studies unable to delimit a clear interspecific boundary between A. sexfasciatus and A. vaigiensis ( Hubert et al., 2012 , 2017 ; Chang et al., 2017). Bertrand et al. (2017) identified a second, less common Indo-West Pacific group of A. vaigiensis as lineage B. Their lineage C is possibly restricted to the Coral Triangle. They did not name the fourth lineage, which was represented by a single GenBank specimen from Christmas Island ( AY208557 ; Quenouille et al., 2004 ). Campbell et al. (2018) subsequently sequenced another individual (labeled as A . cf. vaigiensis ) from Christmas Island (Kiritimati) and confirmed that it is distinct from other putative A. vaigiensis . Our A. vaigiensis , from the eastern coast of Australia (31843 0 12 00 S , 152847 0 54 00 E ), was recovered as the sister group of A. sexfasciatus , a relationship which conforms to Bertrand et al.’s (2017: fig. 2a) mitochondrial tree (cytochrome b ). We conclude that it is a representative of their widespread lineage A. As for which lineage is the true Abudefduf vaigiensis , Bertrand et al. (2017: table S1) only reported lineage B from the type locality, Waigeo, Indonesia (WJC4193–WJC4194, WJC4196; 0825 0 48 00 N , 130849 0 12 00 E ), making it the likeliest candidate. However, lineages A and C also occur in the Coral Triangle, so it is possible that either or both also occur at Waigeo but were not sampled at that location. There is evidence that different lineages can be sympatric; e.g., lineages A and B are found together at Taiping (10822 0 48 00 N , 114822 0 12 00 E; Bertrand et al., 2017: table S1). To further complicate matters, Wibowo et al. (2017) recognized Abudefduf caudobimaculatus as a separate species, removing it from the synonymy of A. vaigiensis . Hensley (1978: 169) remarked on the species status of A. caudobimaculatus , noting ‘‘[t]here is a very real possibility that two species are included’’ in A. vaigiensis , separable into what he called the ‘‘caudobimaculatus’’ and ‘‘vaigiensis’’ groups. Hensley (1978: 247) stated, ‘‘it is likely that future research will show that two species are involved.’’ He provided a suite of characters to differentiate the two forms ( Hensley, 1978 : tables 32–35). Wibowo et al. (2017: 86) suggested that A. caudobimaculatus corresponds to Bertrand et al.’s (2017) lineage B on the basis of a personal communication from an author of the latter paper (W.-J. Chen). This designation has been followed by others (Campbell et al., 2018; Wibowo et al., 2018 ). However, Wibowo et al. (2018) resolved A. caudobimaculatus as the sister group to the rest of Glyphisodon , which this analysis corroborated ( Fig. 1 ). If A. caudobimaculatus is lineage B, that placement would contradict Bertrand et al. (2017: fig. 2), who recovered it either as sister to A. sparoides or lineage C, albeit with weak branch support. If lineage B is indeed the only one to occur at Waigeo, the type locality of A. vaigiensis , then A. caudobimaculatus would need to be returned to the synonymy of A. vaigiensis . Resolving the status of A. vaigiensis and lineages previously identified as such will require further investigation.