Thaperiinae Ota, Reia & Benine

Melo, Bruno F, Ota, Rafaela P, Benine, Ricardo C, Carvalho, Fernando R, Lima, Flavio C T, Mattox, George M T, Souza, Camila S, Faria, Tiago C, Reia, Lais, Roxo, Fabio F, Valdez-Moreno, Martha, Near, Thomas J & Oliveira, Claudio, 2024, Phylogenomics of Characidae, a hyper-diverse Neotropical freshwater fish lineage, with a phylogenetic classification including four families (Teleostei: Characiformes), Zoological Journal of the Linnean Society (Zool. J. Linn. Soc.) 202 (1), pp. 1-37 : 26-28

Thaperiinae Ota, Reia & Benine , new subfamilp

ZooBank: urn:lsid:zoobank.org:act:56486412-0A9F-42B8 BBE2-50E138915341.

Type genus: Ŋayeria Eigenmann, 1908.

Included genera: Bario Myers, 1940 , Bryconamericus (in part), Bryconella Géry, 1965 , Inpaichthys , Hollandichthys Eigenmann, 1910 , Holopristis Eigenmann, 1903 , Hemigrammus (in part), Hyphessobrycon (in part), Parapristella Géry, 1964 , Rachooiscus, Ramirezella Fernández-Yépez, 1949 , and Ŋayeria.

Definition: The least inclusive crown clade that contains Ŋayeria obliqua , Holopristis ocellifer (Steindachner, 1882) , and Inpaichthys kerri Géry and Junk, 1977 . This is a minimum-crown-clade definition. See Figure 7 for a reference phylogeny of Thayeriinae.

Etymology: A patronym for Nathaniel Thayer (1808–1883).

Remarks: The phylogeny inferred from the UCE loci resolves a clade of three species that includes Inpaichthys kerri , Bryconamericus orinocoense Román-Valencia, 2003 , and Hyphessobrycon sp. Jari as the sister-lineage of all other species of Thayeriinae ( Fig. 7). A DNA barcoding study did not resolve B. orinocoense with a clade containing Bryconamericus or other species of Stevardiidae (García-Melo et al. 2019). The undescribed species identified here as Hyphessobrycon sp. Jari has the morphological characteristics consistent with the genus Hyphessobrycon (Eigenmann 1917) but is distantly related to H. compressus . This clade must be investigated further in order to understand the species composition, as many species may be absent from the present study.

There is an interesting clade in Thayeriinae that contains species distributed in Atlantic coastal rivers ( Fig. 7). Hyphessobrycon flammeus Myers, 1924 and H. griemi Hoedeman , 1957 are similar morphologically and found in coastal rivers in

the Atlantic rainforest from Rio de Janeiro to Santa Catarina, Brazil (Weitzman et al. 1988). Hollandichthys multifasciatus (Eigenmann and Norris, 1900) is resolved as the sister-species of Rachooiscus crassiceps Myers, 1926 and R. graciliceps Weitzman and Cruz, 1981 ( Fig. 7), corroborating results from previous phylogenetic analyses ( Quagio-Grassioto et al. 2012, Betancur-R et al. 2019, Mirande 2019, Melo et al. 2022a). Several phenotypic traits are consistent with a close phylogenetic relationship between Hollandichthys and Rachooiscus that includes a unique type of spermiogenesis, presence of a long and spiralling mitochondria in the midpiece of the spermatozoa in both genera, and presence of a ventral body cavity between pelvic and anal fins that houses internally the anus and the urogenital opening in both males and females (Bertaco and Malabarba 2013).

Ramirezella newboldi Fernández-Yépez, 1949 and R. pyrophthalma (Costa, 1994) (former Hemigrammus newboldi and Moenkhausia pyrophthalma ) form a monophyletic group resolved as the sister-lineage of Ŋayeria ( Fig. 7). Ramirezella newboldi was described as a new species and new monotypic genus, initially diagnosed by the presence of scales covering the basal portion of caudal fin, incomplete lateral-line, and short maxilla (Fernández-Yépez 1949). The species was subsequently transferred to Hemigrammus ( Taphorn 1992) , which also highlighted a similar colour paưern shared with Moenkhausia cotinho Eigenmann, 1908 . Recently, Ramirezella newboldi was redescribed and diagnosed from comparisons to M. cotinho (Mathubara and Toledo-Piza 2020) . Moenkhausia pyrophthalma was described by Costa (1994), who hypothesized a close relationship with M. oligolepis (Günther, 1864) , M. sanctaefilomenae (Steindachner, 1907) (herein classified as a species of Bario ; Table 1 ), and M. cotinho based on a reticulate colour paưern, a relationship not supported in the UCE phylogeny ( Fig. 7). Considering that the clade Hemigrammus newboldi and Moenkhausia pyrophthalma is phylogenetically distant from both M. xinguensis (type species of Moenkhausia ) and H. unilineatus (type species of Hemigrammus ), we revalidate Ramirezella Fernández-Yépez, 1949 to include Ramirezella newboldi new combination, and Ramirezella pyrophthalma new combination ( Table 1 ). Ramirezella and Bario possess a reticulate colour paưern, but according to the phylogeny, this feature seems to have evolved independently in these two lineages ( Fig. 7). Moenkhausia cotinho was not included in the UCE phylogenomic dataset, but ongoing research is investigating the phylogenetic placement of this species (L. Reia, unpublished data).

Ŋayeria is unique among characids in that the lower caudal-fin lobe is longer than the upper caudal-fin lobe, there is a dark stripe across the lower caudal-fin lobe that is continuous with a longitudinal stripe, and the body is directed slightly upwards when swimming ( Moreira and Lima 2017). Previous molecular phylogenetic analyses resolved T. boehlkei Weitzman, 1957 and T. ifati Géry, 1959 as a monophyletic group sister to Moenkhausia sanctaefilomenae (Javonillo et al. 2010) . Morphological phylogenetic analysis resolved T. boehlkei and T. obliqua Eigenmann, 1908 as monophyletic based on four synapomorphies, and as the sister-group of Hemigrammus (Mirande 2010) . An expanded morphological dataset of Mirande (2010) resulted in phylogenies where a monophyletic Ŋayeria was the

sister-lineage of a clade containing Petitella bleheri (Géry and Mahnert, 1986) and Petitella georgiae ( Ohara et al. 2017) . The resolution of Ŋayeria in Thayeriinae reflects results from a previous phylogenomic study of UCE loci (Melo et al. 2022a).

Ramirezella and Ŋayeria form a clade sister to a more inclusive group with Bario , some species assigned to Hemigrammus , Parapristella , and Bryconella (fourth to seventh lineages; Fig. 7). With the exception of Bryconella and a few Bario species, which have green to blue eyes when alive, the majority of taxa belonging to this lineage present the upper margin of the eye red in live specimens ( Ohara and Lima 2015).

Bario and several species of Moenkhausia and Hemigrammus skolioplatus Bertaco and Carvalho, 2005 are resolved as a clade of Thayeriinae ( Fig. 7). The genus Bario was described by Myers (1940) asser a complex taxonomic history involving Tetragonopterus lineatus Steindachner, 1891 ( Steindachner 1891). Eigenmann (1893) observed that T. lineatus was preoccupied by a species described by Perugia and replaced it with T. steindachneri Eigenmann, 1893 . Eigenmann (1917) transferred this species to the monotypic genus Entomolepis . Myers (1940) described Bario to replace Entomolepis , since that name was preoccupied in Crustacea ( Entomolepis Brady ). Molecular and morphological phylogenetic studies have shown a close relationship between B. steindachneri and species of Moenkhausia : M. oligolepis , M. sanctaefilomenae , M. forestii Benine et al., 2009 , and M. australis Eigenmann, 1908 (Mirande 2009, 2010, 2019, Mariguela et al. 2013, Melo et al. 2022a). These species comprise the Moenkhausia oligolepis / M. sanctaefilomenae complex (Costa 1994, Lima et al. 2007, Ohara and Lima 2015). The group was defined by a colour paưern characterized by a higher concentration of dark chromatophores in the distal margins of the scales, a vertically elongate humeral blotch, and a conspicuous dark blotch on the caudal peduncle preceded by a lighter area (Costa 1994). Two subgroups in the species complex were proposed based on the degree of flaưening in the pre- and post-pelvic region: laterally compressed in M. australis , M. forestii , M. oligolepis , M. sanctaefilomenae , and Bario steindachneri , and ventrally flattened in M. cosmops Lima et al., 2007, M. uirapuru Ohara and Lima, 2015 , M. diktyota Lima and Toledo-Piza, 2001, and M. lineomaculata Dagosta et al., 2015 ( Reia et al. 2019).

The genus Bario is expanded to include all the eight species analysed here of the M. oligolepis / M. sanctaefilomenae complex ( Fig. 7; Table 1 ). The phylogeny inferred from the UCE loci provides some corroboration for the species groups delimited in Reia et al. (2019), and the UCE phylogeny resolves Bario skolioplatus as the sister-lineage of a clade containing Bario uirapuru and Bario cosmops that was proposed in a previous taxonomic revision ( Ohara and Lima 2015).

One of the clades resolved in the UCE phylogeny is the Hemigrammus ocellifer group that includes H. aguaruna Lima et al., 2016, H. falsus Meinken, 1959 , H. haraldi Géry, 1961 , H. guyanensis Géry, 1959 , H. luelingi Géry, 1964 , H. neptunus Zarske and Géry, 2002 , H. ocellifer , H. pulcher Ladiges, 1938 , and H. yinyang Lima and Sousa, 2009 ( Fig. 7; Lima and Sousa 2009, Lima et al. 2016). Species in this clade possess two humeral blotches, a dark blotch on the caudal peduncle, a red upper eye margin in life, and a single medium-sized hook per anal-fin ray that are arranged in a row along the last unbranched

and seven anteriormost branched anal-fin rays in adult males (Lima and Sousa 2009). Holopristis was described to include Tetragonopterus ocellifer (Eigenmann, 1903) , later synonymized in Hemigrammus (Géry 1959) . Considering the morphological and phylogenomic support for monophyly of this group ( Fig. 7; Lima and Sousa 2009, Lima et al. 2016), we revalidate the genus Holopristis to accommodate Holopristis aguaruna , H. falsus , H. guyanensis , H. haraldi , H. luelingi , H. neptunus , H. ocellifer , H. pulcher , and H. yinyang . Three species of Holopristis were not sampled in the UCE phylogeny: H. falsus , H. luelingi , and H. yinyang .

Species of Parapristella are resolved as a monophyletic group in Thayeriinae ( Fig. 7). Parapristella was described to include P. georgiae Géry, 1964 and Pristella aubynei Eigenmann, 1909 (Géry 1964a). In the UCE phylogeny, Parapristella is resolved as the sister-lineage of a clade containing Bryconella and Hemigrammus oorderwinkleri Géry, 1963 ( Fig. 7). Bryconella is a monotypic genus described to allocate Cheirodon pallidiþons Fowler, 1946 (Géry 1965). Although future studies may suggest that H. oorderwinkleri should be moved to Bryconella , we avoid this transference until further detailed studies are conducted into the taxonomy and phylogeny of species of Thayeriinae. The subfamily contains several clades associated with distinct biogeographic regions. The clade has predominance across the Amazon–Orinoco–Guianas with Bario reaching the La Plata and São Francisco, and the clade with Hyphessobrycon flammeus , H. griemi , Hollandichthys , and Rachooiscus distributed in the Atlantic coastal rivers of eastern Brazil ( Fig. 7).