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Siluriformes: Trichomycteridae), with Comments About Troglomorphism and the Phylogeny of the Genus

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Siluriformes: Trichomycteridae), with Comments About Troglomorphism and the Phylogeny of the Genus JOURNAL OF MORPHOLOGY 278:4–28 (2017) The Laterosensory Canal System in Epigean and Subterranean Ituglanis (Siluriformes: Trichomycteridae), With Comments About Troglomorphism and the Phylogeny of the Genus Pedro Pereira Rizzato1* and Maria Elina Bichuette2 1Laboratorio de Ictiologia de Ribeirao~ Preto, Departamento de Biologia, Universidade de Sao~ Paulo, Ribeirao~ Preto, Sao~ Paulo, Brazil 2Laboratorio de Estudos Subterraneos,^ Departamento de Ecologia e Biologia Evolutiva, Universidade Federal de Sao~ Carlos, Sao~ Paulo, Sao~ Carlos, Brazil ABSTRACT The laterosensory system is a mechano- The canals are ususally embedded in dermal bones sensory modality involved in many aspects of fish biolo- or are surrounded by bony tubes, opening to the gy and behavior. Laterosensory perception may be surface through pores (the laterosensory canal sys- crucial for individual survival, especially in habitats tem; Webb, 2014). The laterosensory system is where other sensory modalities are generally useless, involved in a series of behaviors (Bleckmann, such as the permanently aphotic subterranean environ- ment. In the present study, we describe the laterosen- 1986; Montgomery et al., 2014) and may represent sory canal system of epigean and subterranean species a crucial resource for detection of environmental of the genus Ituglanis (Siluriformes: Trichomycteridae). stimuli in the absence of other sources of sensory With seven independent colonizations of the subterra- information, as is seen in fishes living in subterra- nean environment in a limited geographical range cou- nean habitats or other aphotic environments. pled with a high diversity of epigean forms, the genus Trichomycteridae (Teleostei: Ostariophysi: Silur- is an excellent model for the study of morphological iformes; Fig. 1) is the third richest family in terms specialization to hypogean life. The comparison of number of known exclusively subterranean fish- between epigean and subterranean species reveals a es (Rizzato and Bichuette, 2014). The family is a trend toward reduction of the laterosensory canal sys- tem in the subterranean species, coupled with higher monophyletic assemblage of small catfishes easily intraspecific variability and asymmetry. This trend is diagnosed by their highly specialized opercular- mirrored in other subterranean fishes and in species interopercular apparatus bearing odontodes (de living in different confined spaces, like the interstitial Pinna, 1998; de Pinna and Wosiacki 2003; environment. Therefore, we propose that the reduction Adriaens et al., 2010; Datovo and Bockmann, of the laterosensory canal system should be regarded 2010). Species in this clade show a high diversity as a troglomorphic (5 cave-related) character for sub- of diet types and life habits (Datovo and Bock- terranean fishes. We also comment about the patterns mann, 2010), including parasitic or semi-parasitic of the laterosensory canal system in trichomycterids habits (especially in the more derived subfamilies, and use the diversity of this system among species of Ituglanis to infer phylogenetic relationships within the for example, the mucus and scale-eating stegophi- genus. J. Morphol. 278:4–28, 2017. VC 2016 Wiley Periodi- lines and the hematophagous vandellines), and the cals, Inc. KEY WORDS: lateral line; troglobite; cavefish; cave Additional Supporting Information may be found in the online adaptation; morphological evolution version of this article. Contract grant sponsor: Sao~ Paulo Research Foundation (FAPESP); Contract grant number: 2010/08459-4 (MEB), 2009/ INTRODUCTION 15030-7 (PPR), 2011/06736-3, and 2011/15429-7. The neuromast-based mechanoreceptive latero- *Correspondence to: Pedro Pereira Rizzato, Avenida Bandeir- sensory system in teleosts (sensu Webb, 1989) con- antes, 3900, Monte Alegre, Ribeirao~ Preto, Sao~ Paulo, Brazil 14040- sists of lines of sensory organs, the neuromasts, 901. E-mail: [email protected] which detect and react to mechanical stimuli pro- duced by water displacement (Dijkgraaf, 1962; Received 16 December 2015; Revised 31 August 2016; Montgomery et al., 1995; McHenry and Liao, Accepted 6 September 2016. 2014). Such structures may be present in shallow Published online 21 October 2016 in pits or grooves in the skin surface (the superficial Wiley Online Library (wileyonlinelibrary.com). neuromasts), or inside pored, subepidermal canals. DOI 10.1002/jmor.20616 VC 2016 WILEY PERIODICALS, INC. LATEROSENSORY CANAL SYSTEM OF ITUGLANIS 5 focus of studies of convergent evolution of cave- related characters in subterranean fishes. Arratia and Huaquin (1995) described the latero- sensory canals of representatives of most genera of Trichomycterinae, except for Ituglanis. Since the work of Datovo and Landim (2005), descriptions of the laterosensory canals and pores have been included in taxonomic works for all new species of Ituglanis described or redescribed so far: I. macu- naima (Datovo and Landim, 2005); I. cahyensis (Sarmento-Soares et al., 2006); I. paraguassuensis Fig. 1. Cladogram depicting the relationships between the sub- (Campos-Paiva and Costa, 2007); I. amazonicus, I. families of Trichomycteridae, as well as the composition of the parkoi, plus four undescribed species from the Ama- clades “C” and “TSVSG” that are refered to in literature and in zon basin (Canto, 2009); I. ina (Wosiacki et al., the present work. The topology was based on the work from 2012); I. agreste (Lima et al., 2013); I. apteryx Datovo and Bockmann, Neotrop Ichthyol, 2010, 8, 193–246, reproduced by permission. The eight genera of Trichomycterinae (Datovo, 2014); I. australis (Datovo and de Pinna, are highlighted on the inset. 2014); I. boticario (Rizzato and Bichuette, 2014); I. boitata (Ferrer et al., 2015); and I. goya (Datovo et al., 2016). Sarmento-Soares et al. (2006) also pro- vide a description of the laterosensory canal system successful colonization of unusual habitats, such of I. proops and I. parahybae. Some of these studies as the subterranean environment (Rizzato and use the pattern of canals and pores of the laterosen- Bichuette, 2014). sory system to diagnose species (Datovo and All but two of the known subterranean species Landim, 2005; Sarmento-Soares et al., 2006; Lima of trichomycterids are included in its most speciose et al., 2013; Datovo, 2014; Datovo and de Pinna, subfamily, the Trichomycterinae (sensu Datovo 2014; Rizzato and Bichuette, 2014; Ferrer et al., and Bockmann, 2010; Fig. 1), which includes the 2015; Datovo et al., 2016). genera Bullockia, Eremophilus, Hatcheria, Rhizo- In the present work, we describe the general pat- somichthys, Scleronema, Silvinichthys, and the tern of laterosensory canals for Ituglanis, comment most species-rich Trichomycterus and Ituglanis. about the diversity of this system among epigean The genus Trichomycterus is also the richest tri- and subterranean species, and analyze the intraspe- chomycterid genus in the number of known sub- cific and intraindividual variability with respect to terranean representatives, with 13 species canals and segments of canals, especially in subter- distributed in caves from Brazil, Colombia, Vene- ranean species. With these data, and using Itugla- zuela, and Bolivia, followed by Ituglanis, with sev- nis as a model, we discuss the relationship between en subterranean species known to date, all of the variability and reduction of the laterosensory which occur in Brazilian caves (Rizzato and Bichu- canal system and the subterranean life habit of fish- ette, 2014). es in general. We also include comments about the The seven subterranean species of Ituglanis: I. phylogenetic relationships among the species of Itu- passensis, I. bambui, I. epikarsticus, I. ramiroi, I. glanis, using inferences provided by the diversity of mambai, I. boticario, and an undescribed species the laterosensory csnal system within the genus. from caves in the Posse municipality (Goias state, Brazil), Ituglanis sp. “Posse”, are of special inter- est for both geographical and evolutionary rea- MATERIALS AND METHODS sons. These species occur in a very limited We collected data about the laterosensory system of canals geographic range, the northeastern portion of for 24 of the 26 described species of Ituglanis—the exceptions Goias state, Brazil, where two large carbonate (5 were I. guayaberensis (Dahl, 1960) and I. laticeps (Kner, 1863)—including the six described subterranean species, plus 1 limestone) karst areas occur, the Sao~ Domingos, to undescribed subterranean species (Ituglanis sp. “Posse”). Addi- the north, and the Mambaı, to the south (see map tionally, we included data from three species of Trichomycterus: and details in Rizzato and Bichuette, 2014). There T. brachykechenos (Ferrer and Malabarba, 2013); T. cachiraen- is evidence that the colonization of the subterra- sis (Ardila-Rodrıguez, 2008); and T. steindachneri (DoNasci- nean environment occurred independently for each miento et al., 2014a,b). These three species were recently proposed to be closely related to the genus Ituglanis (DoNasci- of these species. Collectively, they show a mosaic miento et al., 2014b), based on a supposed morphocline in rela- of troglomorphic (5 cave-related) features with the tion to the reduction of the cranial fontanel, and they are overall more troglomorphic species, I. passensis, I. included here as an outgroup for comparison. bambui, I. epikarsticus, and I. ramiroi occuring in Data from species of Ituglanis were obtained from direct the Sao~ Domingos karst area, while the less trog- examination of alcohol-preserved
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