Lugubria, Varella & Kullander & Menezes & Oliveira & López-Fernández, 2023

Varella, Henrique R, Kullander, Sven O, Menezes, Naércio A, Oliveira, Claudio & López-Fernández, Hernán, 2023, Revision of the generic classification of pike cichlids using an integrative phylogenetic approach (Cichlidae: tribe Geophagini: subtribe Crenicichlina), Zoological Journal of the Linnean Society 198 (4), pp. 982-1034 : 1022-1026

Node 130— Lugubria , new genus u r n: l s i d: z o o b a n k. o r g: a c t: D 7 5 8 B0 1 C - 2A 6 6-

4402-B63D-A20FDA199C96

Type species: Crenicichla lugubris Heckel, 1840 .

Lugubria is recovered with high support in the ML and BI trees (BS100%, PP 100%) but low support in the parsimony analysis based on EW/DiscreteMatrixTE (ABS 6/RBS 25%; Table 6). The genus comprises 16 valid species and corresponds to the Crenicichla lugubris group of Kullander (1991, 1997; excluding Crenicichla vittata ) and Ploeg (1991; excluding C. vittata and C. jegui ; Fig. 3I). This group has been recovered by previous studies based on phylogenomics and good taxonomic coverage (Burress et al. 2017, 2018; Fig. 3D–F). Fourteen unambiguous molecular transformations and 15 morphological synapomorphies (nine of them unambiguous) are optimized for the genus ( Table 17).

Diagnosis: Lugubria includes species with relatively large body (max. SL 225–300 mm) distinguished from all other pike cichlids by the combination of reduced size of the scales in the whole body reflected in the high number in the E1 row (88–123 scales; see Remarks), the high count of soft rays in the dorsal and anal fins (13–18 and 9–13, respectively), and the high number of vertebrae (39–44 vertebrae). Crenicichla (Lacustria) vittata is similar to species of Lugubria by having high counts of vertebrae and scales in the E1 row but differs from all species of that genus by females showing orange or reddish pigmentation on the lateral portion of the abdomen, whereas in species of Lugubria this pattern is not observed—in most species, sexually dimorphic females have a broad reddish or purplish broad pigmentation on the ventral portion of the abdomen (belly). Crenicichla (Lacustria) vittata also shows a suborbital marking composed of distinct dark spots that together form a stripe, which is characteristic of other species of the subgenus Lacustria of Crenicichla , whereas species of Lugubria do not show suborbital marking or have it uniformly pigmented. Finally, most species of Lugubria show a dark blotch posterior to the pectoral fin that appears only late during ontogeny and is absent in C. (La.) vittata .

Species of Lugubria are further distinguished from Saxatilia by the absence (vs. presence) of a humeral blotch that appears early in ontogeny and remains in adults; from Hemeraia and Teleocichla by having all post-lachrymal infraorbitals autogenous (vs. infraorbitals 4 and 5 co-ossified) and posterior margin of preopercle strongly serrated (vs. preopercle smooth or with weak serrations irregularly distributed along the posterior margin); and from Wallaciia by the absence (vs. presence) of serrations on the posterior margin of the supracleithrum. Species of Lugubria are additionally distinguished from the subgenus Crenicichla by having all scales on head cycloid (vs. scales ctenoid on cheek and predorsal area) and by the presence (vs. absence) of a dark blotch on the caudal fin, with the exception of Lugubria johanna and Lu. monicae , which lack the caudal fin blotch. Species of Lugubria are futher distinguished from all species of the subgenus Batrachops of crenicichla, except C. (B.) jegui , by the absence of a reticulate pattern of coloration on the flank (vs. presence of a reticulate pattern resulting from the dark pigmentation on the base of each scale on the flank).

Distribution: Lugubria is distributed in all major tributaries of the Amazon basin, in the Río Orinoco basin, and coastal drainages of the Guianas. There are no records of Lugubria in the Atlantic coastal drainages or the La Plata basin.

Remarks: Since Kullander (1991, 1997), species of the C. lugubris group have been subdivided into the C. acutirostris group and C. lugubris group s.s. (e.g. Montaña et al. 2008; Kullander and Varella 2015). Crenicichla (Lacustria) vittata and C. (Batrachops) jegui were tentatively allocated in the C. acutirostris group, which has recently been contested ( Piálek et al. 2012; Burress et al. 2017, 2018; this paper; see Fig. 3). The distinction between these subgroups was based on a series of characters in combination, including a depressed head and long, pointed snout in the C. acutirostris group, with nostril halfway between the postlabial skin fold and the anterior margin of orbit vs. blunt snout in the C. lugubris group s.s., with nostril closer to postlabial skin fold, as well as some details of coloration related to ontogeny. All analyses performed herein recover a Lu. lugubris group s.s. ( Node 137) as monophyletic. Among the synapomorphies for this group, some are related to the blunt snout (char. 13: 1=>0 and char. 96: 0=>1) and the changes on the coloration during ontogeny, i.e. the presence of dark spots scattered on the anterior portion of the body (in juveniles) and the presence (in adults) of a dark blotch posterior to the pectoral fin and another on the pectoral axilla (chars. 70: 0=>1; char. 71: 0=>1; and 81: 0=>1). The Lu. acutirostris group sensu Kullander (1991 , 1997), including all long-snout species of Lugubria , is recovered only in the parsimony analyses under extended implied weighting but not recovered in our main hypothesis (ML tree), in the BI tree and in the parsimony analyses under equal weighting.

CHARACTER CONGRUENCE AND INSIGHTS ON PHENOTYPIC DIVERSIFICATION

Discussions on macroevolution of the clade of pike cichlids (subtribe Crenicichlina ) have been focused on the subgenus Lacustria of Crenicichla , which is restricted to the rivers of southern South America ( Piálek et al. 2012, 2019a; Burress et al. 2017, 2018). These studies suggest the existence of adaptive radiations in the C. (La.) missioneira complex in the Río Uruguay and of the C. (La.) mandelburgeri complex in the Río Paraná. Except for their occurrence in complex riverine (instead of lacustrine) habitats, these radiations were considered similar to the species flocks in the African Great Lakes and Middle America ( Piálek et al. 2012), i.e. monophyletic assemblages of closely related species (shallow genetic divergence) that coexist in the same area with a high level of endemicity and ecomorphological specialization.

Our results agree with these previous studies in demonstrating the occurrence of parallel evolution of ecomorphological traits in geographically isolated habitats between the C. missioneira and C. mandelburgeri complexes, most of them related to feeding and microhabitat occupation (e.g. Burress et al. 2018; Piálek et al. 2019a). Several characters present in these clades correlated to rheophyly and durophagy were highly homoplastic among pike cichlids. These characters were clearly homoplastic and phylogenetically misleading when morphological characters were analysed alone, resulting in lack of resolution and long-branch attraction.

More generally, ecomorphological convergence is rampant beyond the well-known cases within the subgenus Lacustria , with clear examples among multiple pike cichlid taxa coexisting in complex environments such as rapids. Examples are the assemblages comprising C. (B.) jegui , C. (B.) cametana , and C. (B.) cyclostoma occurring in sympatry in rapids of the Río Tocantins basin and the diverse assemblages of Teleocichla and Lugubria in rapids of the Río Xingu basin. Varella et al. (2018) discussed characteristics related to microhabitat occupation and feeding within the assemblage of Teleocichla from the Río Xingu, most of them reanalysed herein in a phylogenetic framework and confirmed as convergent. Likewise, Varella and Ito (2018) explored the large diversity of the C. lugubris group (= Lugubria ) in the Río Xingu basin and highlighted the convergent dark coloration between Lugubria dandara , Teleocichla preta , and Crenicichla (La.) hu, which is comparable to that of Crenicichla (B.) cyclostoma and C. (B.) cametana . Dark coloration in these species might be understood as a convergent adaptation for inhabiting swift, clear-water rapids over beds of dark rocks widespread in the Brazilian Shield.

On the other hand, the diversity of the genera Lugubria , Saxatilia , and Wallaciia and of the subgenus Batrachops of Crenicichla suggest widespread allopatric divergence resulting in ecomorphologically similar species across river basins. Most species or populations within their widespread species (see: Říčan et al. 2021a) are distributed following hydrography or geological history. In these groups, there is widespread variation in sexually selected traits (sexual dimorphism and dichromatism), but traits associated with feeding or habitat occupation vary much less, with ecomorphological variation mostly restricted to pairs or small groups of sympatric species living in fast current environments.

From our study, it remains unclear if sympatric assemblages diversified in situ (like those of Lacustria radiations in the Uruguay and Paraná rivers), because our taxonomic sampling, character coding, and analyses focused on assessing monophyly clarifying relationships among the major groups of pike cichlids, sacrificing resolution of less-inclusive groups. The taxonomic sampling of recent phylogenomic analyses ( Piálek et al. 2012, 2019a; Burress et al. 2017, 2018) also prevents inference of relationships within these less studied sympatric assemblages. Nevertheless, Říčan et al. ’s (2021a) recent study using a large taxonomic sampling but only two mtDNA markers suggests monophyly of the assemblage of Lugubria in the Río Xingu basin and of Crenicichla (Batrachops) in the Río Tocantins basin, but not of the large sympatric assemblage of Teleocichla in the Río Xingu basin. Říčan et al. (2021a, b) studies also suggest the existence of smaller sympatric groupings of Crenicichla (Lacustria) that evolved parallel ecomorphs in different rivers basins of the Río Paraná basin.

In that context, resource partitioning apparently plays an important role in the origin or maintenance of the phenotypic diversity among rheophilic pike cichlids in different river basins or, more generally, among coexisting but phylogenetically distant species that occupy more or less specialized ecological niches. Moreover, resource partitioning apparently plays a role even within the already specialized rheophilic assemblage of Teleocichla in the Río Xingu (Zuanon 1999; Varella et al. 2016). From this perspective, the role of ecological speciation may be a fruitful avenue for subsequent studies on the evolution of pike cichlids beyond the C. (La.) missioneira and C. (La.) mandelburgeri complexes. Recent studies with broader taxonomic scope (e.g. Arbour and López-Fernández 2014; Astudillo-Clavijo et al. 2015) place the phenotypic and funcional diversification of pike cichlids in the broader context of the tribe Geophagini and Neotropical cichlids, highlighting that pike cichlids occupy a vast and largely unique functional morphospace among their South American relatives. However, because few representatives of pike cichlids were included in these analyses, much about the evolution within the clade remains unexplored and will be the subject of future studies.