A state-of-art review of Loricariidae (Ostariophysi: Siluriformes) cytogeneticsAbstract
Loricariidae is a Neotropical fish family divided into six subfamilies and ranking in third among the most biodiverse fish groups. This study conducts an updated review of the cytogenetic investigations within the family, discussing the trends in chromosomal evolution and the main gaps and future directions for studies. Covering 125 publications that analyzed 234 species from all subfamilies except Lithogeninae, corresponding to about 21% of the valid species diversity, our study revealed samples from six different river basins in Argentina, Brazil, Ecuador, Paraguay, and Venezuela. There was a dearth of data for northeast Brazil, the Western Amazon, the Guianas Shield, and other Neotropical countries. In loricariids, there are seven different sex chromosome systems and a variety of diploid numbers (2n) ranging from 33 to 96 as a result of different chromosomal rearrangements such as fusions, fissions, translocations, and inversions. We recorded more simple nucleolar organizer regions (Ag-NOR) compared to multiple ones, and the fundamental number (FN) varied between 34 and 142. Populational studies have been conducted only in a few taxa, but a remarkable karyotype variation that includes B chromosomes is shown. Despite continuous efforts, cytogenetics still does not adequately capture the diversity of Loricariidae.
Keywords:
Ag-NOR; B chromosomes; Karyotype; Plecos; Sex chromosomes
Resumo
Loricariidae é uma família de peixes Neotropicais dividida em seis subfamílias e ranqueada na terceira posição dentre os grupos mais biodiversos de peixes. Este estudo conduz uma revisão atualizada das investigações citogenéticas na família, discutindo as tendências evolutivas cromossômicas e as principais lacunas e direções futuras para estudos. Cobrindo 125 publicações que analisam 234 espécies de todas as subfamílias, exceto Lithogeninae, correspondendo a aproximadamente 21% da diversidade de espécies válidas, nosso estudo revelou amostragens em seis bacias hidrográficas distintas na Argentina, Brasil, Equador, Paraguai e Venezuela. Há uma escassez de dados para o nordeste do Brasil, o oeste da Amazônia, o escudo das Guianas e outros países Neotropicais. Em loricariídeos, há sete sistemas de cromossomos sexuais distintos e uma variedade de números diploides (2n), variando de 33 a 96 como resultado de rearranjos cromossômicos diferentes como fusões, fissões, translocações e inversões. Nós registramos mais regiões organizadoras de nucléolo (Ag-RON) simples quando comparado com múltiplas, e o número fundamental (NF) variou entre 34 e 142. Estudos populacionais foram realizados em poucos organismos, mas uma extraordinária variação cariotípica que inclui cromossomos B é demonstrada. Apesar de esforços contínuos, a citogenética ainda não captura adequadamente a diversidade de Loricariidae.
Palavras chave:
Ag-RON; Cariótipo; Cascudos; Cromossomos B; Cromossomos sexuais
INTRODUCTION
Among vertebrates, the paraphyletic group of fish outstands because of its high richness and diversity of morphology and ecology (Nelson et al., 2016). They can be found all over the Earth in freshwater and marine environments, and humans exploit them widely as primary food sources or as ornamental species for the aquarium trade (Evers et al., 2019; Novák et al., 2020, 2022). Such diversity is observed in about 36,000 valid species, with almost half of them belonging to the 450 families that make up the infraclass Teleostei (Fricke et al., 2023). More than 18,000 species are found in freshwater environments, the majority of which are found in tropical and subtropical regions, including the Amazon River Basin, tropical Africa, and southeast Asia (Lévêque et al., 2008; Nelson et al., 2016). The monophyletic order Siluriformes (popularly known as catfishes), is home to a large portion of this variety (Fink, Fink, 1981, 1996; Arratia et al., 2003; Saitoh et al., 2003; Sullivan et al., 2006). This order is composed by the suborder Loricarioidei, which consists of six families that are endemic to South America, and Siluroidei, which includes 29 families that are spread over all continents except Antarctica (Sullivan et al., 2006). Due to their widespread distribution (Fig. 1), research focusing on the biogeography of siluriform fishes often indicates that South America may have served as the group’s center of origin (Briggs, 2005; Sullivan et al., 2006).
Loricariidae species, which rank third among the most biodiverse fish families, are known by several names, including armored catfishes, plecos, “cascudos”, “bodós”, and “acaris”. Together with Characidae and Cyprinidae, it corresponds for about 50% of all Ostariophysi species (Nelson et al., 2016). According to Fricke et al. (2023), 1,051 valid species are divided into six subfamilies: Delturinae, Hypoptopomatinae, Hypostominae, Lithogeninae, Loricariinae, and Rhinelepinae. Their distinct anatomy, which includes a suckermouth positioned ventral and dermal plates covering the body, allows them to be recognized despite their widespread distribution in the Neotropical region. Loricariids are iliophagous, with a vast diversity of feeding habitats ranging from wood to detritus and algae (Buck, Sazima, 1995; Lujan et al., 2017). They demonstrate a broad range of sizes, from less than 5 cm (e.g., Ribeiro et al., 2012) to approximately 1 m (Lujan et al., 2010). Given a combination of excessive reaping for the aquarium trade and the destruction of their habitats, some loricariids are threatened (Barros et al., 2023). Indeed, the high ornamental trade of plecos led to the development of the L-code (or L-number). This code was developed by aquarists, aiming to create a temporary “voucher number” for morphological variants identified by aquarium trade that lack a proper taxonomic identification or are difficult to classify only by morphological features (Stawikowski et al., 2004). Recently, 223 Loricariidae species have been assigned from their L-numbers to valid species name (Novák et al., 2022).
World map showing the distribution of Siluriformes (red areas) according to Nelson et al. (2016) and GBIF (2023), with illustrations of important families in distinct regions.
The description of fish species is often complex. While some species present a conservation of morphological features, body-color variation and polymorphisms are frequently observed in fish (Price et al., 2008). In this context, the use of complementary methods is fundamental to assessing all biodiversity, in especial cytogenetics (Stace, 2000), the field of genetics that studies chromosomes from their structure and molecular composition to their organization and variation among species. Cytogenetics is an important tool for discovering the Neotropical fish biodiversity, as exemplified by the outstanding number of new and/or cryptic species in addition to karyomorphs with absence of hybrid forms reported (e.g., Pazian et al., 2012; Ferreira et al., 2014; Oliveira et al., 2006; Ramirez et al., 2017; Rocha-Reis et al., 2018). Among loricariids, Artoni, Bertollo (2001) suggest that 2n = 54 might represent the basal diploid number for this family, with distinct trends in evolution among its subfamilies. Considering the continuous growing number of studies involving Loricariidae species, here we review for the first time the scientific literature that includes cytogenetic data for Loricariidae species. We discussed the trends in chromosomal evolution in this representative fish group and the main gaps and future directions for studies.
MATERIAL AND METHODS
A detailed search was conducted on Google Scholar until December of 2023, using the keywords “Cytogenetics Loricariidae” and “Chromosomes Loricariidae”. During the screening of research papers, all the duplicate papers and cytogenetic papers without karyotype information were excluded from our compilation (for example Traldi et al., 2019, where only mapping of repetitive sequences was conducted, without addressing the diploid number — 2n and karyotype structure). We included all papers found published between 1968 and 2023 in journals in any language available. For more assurance on the quality of results, the data analyzed was double-checked by the authors: the resulted table comprising the cytogenetic features was checked by each author, comparing with the original papers to determine whether such articles would comply with the inclusion and exclusion criteria. We followed the classification of chromosomes by the centromeric position and arm ratios, proposed by Levan et al. (1964) and standardized for fish in Arai (2011) as metacentric (m), submetacentric (sm), subtelocentric (st) and acrocentric (a).
From each paper, we extracted cytogenetic and biogeographic data such as diploid number (2n), fundamental number (NF), karyotype formula (KF), sex chromosome system (SCS) and AgNOR/18S rDNA sites (simple or multiple). Additionally, locality and geographical coordinates of the populations investigated were also compiled, with the city name, state, and country indicated according to the coordinates provided in the papers. Species and family names were checked against Eschmeyer’s Catalog of Fishes (Fricke et al., 2023) and updated according to the valid names. Taxonomic abbreviations were maintained as present in the papers, following: “sp.” for specimens not fully identified, “prope” for specimens with resemblance to a described taxon but not identical, “aff.” for closely related to an identified taxon or with uncertainty in taxonomic identification, “cf.” for specimens similar to or comparable to a taxon but with doubts, “n.sp.” for proposed new species, and “L.” for locally variants of specimens. For the papers in which the geographical coordinates were available, we plotted those sample points into maps using QGIS 3.28.2.
RESULTS
We compiled 125 papers that included cytogenetic data on Loricariidae species. These studies comprised a diversity of 234 species, here included those identified as “sp.”, prope, “aff.”, “cf.”, “n.sp.”, and “L” as distinct species, from 48 genus. Hypostominae was the subfamily most represented with 142 species karyotyped, followed by Loricariinae (54 spp.), Hypoptopomatinae (34 spp.), and Delturinae and Rhinelepinae with 2 spp. each, with absence of data for Lithogeninae. The Hypostomus genus was the most represented with 26 valid species karyotyped, in a total of 159 records when including all populational data and those identified as “sp.”, prope, “aff.”, “cf.”, “n. sp.”, and “L”. The geographical coordinates plotted into maps show a distribution of species cytogenetically investigated in Brazil, Argentina, and Paraguay, comprising six distinct river basins (Fig. 2). Although species from Ecuador and Venezuela were also compiled, those papers do not present geographical coordinates of the sample sites.
Diploid number varied from 2n = 33 in males of Rineloricaria teffeana (Steindachner, 1879) (Marajó et al., 2022) to 2n = 96 in Hemipsilichthys sp. (Kavalco et al., 2004, 2005). The fundamental number ranged from 34 in R. teffeana (Marajó et al., 2022) to 142 in Hypostomus topavae (Godoy, 1969) (Kamei et al., 2017), and the simple distribution of Ag-NOR/18S rDNA was the most common with 269 records, against 110 records of multiple sites. Seven sex chromosomes systems were described for 31 Loricariidae species, the simple XX/XY, XX/X0, and ZZ/ZW, and the multiples X1X1X2X2/X1X2Y, XX/XY1Y2, ZZ/ZW1W2, and Z1Z1Z2Z2/Z1Z2W1W2. B chromosomes were found in five species, varying from 1B (e.g., de Souza et al., 2009) to 3B chromosomes (e.g., Porto et al., 2010). Complete results were compiled in Tab. 1.
Partial maps of South America showing the distribution of Loricariidae species (red dots) investigated by cytogenetics that have the geographical coordinates published together. A. Map highlighting the geopolitical regions of South America, with emphasis on Brazil, Paraguay, and part of Argentina territory; B. Map highlighting the hydrographic basins of South America, with emphasis on Amazonas (green), Tocantins-Araguaia (yellow), Paraná/Paraguay (purple), São Francisco (cyan), Atlantic East and Atlantic South (red) River Basins.
Review of cytogenetic data by subfamily of Loricariidae published as articles. Geographical coordinates ending with asterisk indicates mismatched coordinates. Diploid number (2n), fundamental number (NF), karyotype formula (KF), sex chromosome system (SCS) are displayed.
DISCUSSION
The origin of the chromosomal diversity of Loricariidae is attributed to both ecological and molecular factors. Small and isolated populations, in addition to the low vagility, are the main ecological characteristics that have allowed the fixation of chromosomal rearrangements in Loricariidae, as suggested for Farlowella (Marajó et al., 2018), Harttia (Sassi et al., 2023), and Rineloricaria (Rosa et al., 2012). The diploid number 2n = 54 is often considered the ancestral diploid number for the family, since it is observed in most Loricariidae subfamilies and present in other Siluriformes (Artoni, Bertollo, 2001). However, there is no consensus on the matter particularly considering the new karyotypic description of basal taxa within subfamilies. Takagui et al. (2020) in a review of Loricariinae karyotypes argue that although predominant, 2n = 54 should not be considered the basal diploid number for the family because multiple divergences in the microstructure of karyotypes within the same 2n are recurrently seen throughout the family. Notably, the 2n range in Loricarioidei suggest that other numbers rather than 2n = 54 can be considered the plesiomorphic ones, as Astroblepidae presents 2n = 52–54, Scoloplacidae 2n = 50, Callichthyidae 2n = 40–134, and Trichomycteridae 2n = 32–62 (reviewed by Conde-Saldaña et al., 2018). Beyond that, the Diplomystidae (Siluroidei) presents 2n = 56 chromosomes (Campos et al., 1997; Oliveira, Gosztonyi, 2000), which might also suggest that as the ancestral 2n.
We plotted the 2n range per subfamily into the main molecular phylogenetic reconstructions of Loricariidae (Fig. 3) and 2n = 54 is the most widespread, being conserved in Rhinelepinae and present in all other subfamilies. Regardless matter whether 2n = 54 or 2n = 56 is the ancestral diploid number, it is noteworthy that chromosomal evolution in Loricariidae is complex. Considering the lower number of karyotyped species when compared to the valid richness, 234 spp. with cytogenetic data against 1,051 valid species (Fricke et al., 2023), it is difficult to establish the evolutionary pathways that led to the observed variability. Notably, while the stability is restricted to 2n in some genera, with high divergence in karyotype structure, as the 2n = 58 in Farlowella, 2n = 54 in Corumbataia, and 2n = 52 in Pterygoplichthys, stable 2n and karyotype is also observed, as the 2n = 52 (26m+20sm+6st/a) in two species of Panaque. Our compilation reveals that processes of ascending and descending dysploidy (i.e., the increase or decrease of 2n while preserving the genomic content) were frequent in most subfamilies but Rhinelepinae, which may exhibit the constant 2n = 54 as a symplesiomorphic trait.
Despite the 2n conservation in Rhinelepinae, variations in the karyotype structure are observed within and between species. Populations of Rhinelepis aspera Spix & Agassiz, 1829 from the same river differ in the karyotype formula (Artoni, Bertollo, 2001; Endo et al., 2012), suggesting that pericentric inversions played an important role in the chromosomal evolution of the species. Such mechanism is not restricted to Rhinelepinae but also observed in other loricariids, such as Ancistrus (Mariotto et al., 2009), Loricariichthys (Takagui et al., 2014), and Rineloricaria (Rosa et al., 2012; Primo et al., 2018). In addition, the multiple Ag-NOR observed in Pogonopoma wertheimeri (Steindachner, 1867) (Artoni, Bertollo, 2001) when compared to the simple distribution in other Rhinelepinae species suggest that other mechanisms are also important for the chromosomal evolution in the group. Notably, numeric and structural polymorphisms are frequently observed in loricariids, for example in the multiple karyomorphs of Rineloricaria pentamaculata Langeani & de Araujo, 1994 (Glugoski et al., 2023), and the presence of B chromosomes in Harttia longipinna Langeani, Oyakawa & Montoya-Burgos, 2001 (Blanco et al., 2012). This chromosomal diversity was probably generated by a combination of rearrangements that include Robertsonian fusions and fissions, paracentric and pericentric inversions, and translocations (Artoni, Bertollo, 2001; Kavalco et al., 2004; Ziemniczak et al., 2012).
Phylogenetic relationships of Loricariidae with cytogenetic data herein compiled in red. Molecular phylogenies modified from: A.Roxo et al. (2014); B.Lujan et al. (2015); C. , Pereira, Reis (2017); D. Roxo et al. (2019).
Although rare in most fish species, being observed in only about 5% of Teleostei species (Arai, 2011; Sember et al., 2021), our compilation shows that Loricariidae species carry seven out of the nine known sex chromosome systems observed among fishes. Ancistrus was demonstrated to harbor the largest diversity of sex chromosomes with six of the seven recognized systems for the family distributed in 18 species, corresponding to about 23% of the valid species (Neuhaus et al., 2023). The simple XX/XY was the most predominant in the genus, recorded in A. maximus de Oliveira, Zuanon, Zawadzki & Rapp Py-Daniel, 2015 (Oliveira et al., 2010; Favarato et al., 2016), Ancistrus cf. dubius (Mariotto et al., 2011), Ancistrus sp. 1 Quianduba River (Silva et al., 2022, 2023), Ancistrus sp. 1 Maracapucú River (Santos da Silva et al., 2023), Ancistrus sp. 1 Ilha do Capim (Santos da Silva et al., 2023), Ancistrus sp. Catalão (Favarato et al., 2016), Ancistrus sp. L2 (Prizon et al., 2017), Ancistrus sp. L3 (Prizon et al., 2017), and Ancistrus sp. Purus (Oliveira et al., 2010; Favarato et al., 2016). Additionally, two multiple sex chromosome systems that were not observed in any other Loricariidaeare recorded in Ancistrus: ZZ/ZW1W2 in A. clementinae Rendahl, 1937 (Nirchio et al., 2023), and Z1Z1Z2Z2/Z1Z2W1W2 (Oliveira et al., 2008; Favarato et al., 2016). On other hand, Harttia harbor the highest number of multiple sex chromosome systems when compared to the number of valid species, with six occurrences representing about 25% of valid species (compiled in Sassi et al., 2021): XX/XY1Y2 in H. carvalhoi Miranda Ribeiro, 1939, H. intermontana Oliveira & Oyakawa, 2019, and Harttia sp. 1 (Centofante et al., 2006; Deon et al., 2020); X1X1X2X2/X1X2Y in H. duriventris Rapp Py-Daniel & Oliveira, 2001, H. punctata Rapp Py-Daniel & Oliveira, 2001, and H. villasboas Oyakawa, Fichberg & Rapp Py-Daniel, 2018 (Blanco et al., 2014; Sassi et al., 2020), in addition to putative simple XX/XY in H. rondoni Oyakawa, Fichberg & Rapp Py-Daniel, 2018 and H. torrenticola Oyakawa, 1993 (Deon et al., 2020; Sassi et al., 2020). The Loricariidae diversity of sex chromosomes was originated by rearrangements that include translocations (Blanco et al., 2014), centric fissions (Sassi et al., 2023); centric fusions (Centofante et al., 2006), and pericentric inversions (Artoni et al., 1998), including the combination of distinct rearrangements especially in the origin of multiple sex chromosome systems (Oliveira et al., 2008; Deon et al., 2022). Sex chromosomes in Loricariidae seems to have independent origins, but further research is required to explore the genomic content of those sex chromosomes and its origin. Indeed, there is a recognized lack of information regarding the effects of environmental cues and molecular/gene mechanisms in sex determination of Neotropical fishes (Fernandino, Hattori, 2019).
Most Loricariidae species present a single 18S rDNA/Ag-NOR site, which is also considered a plesiomorphic character in the group (Artoni, Bertollo, 2001; Kavalco et al., 2004), and the standard distribution in most vertebrates (Sochorová et al., 2018). Notably, such region in loricariids is involved in several chromosomal rearrangements, including the origin and differentiation of sex chromosomes, being considered evolutionary breakpoint regions in Ancistrus, Harttia, and Rineloricaria (Glugoski et al., 2018; Deon et al., 2022). Size heteromorphism in the Ag-NOR site is also common, probably because of unequal crossing-over between homologs (Takagui et al., 2020). According to our review, some genus conserved the simple Ag-NOR locus in all analyzed species to date (here included only those genera with more than one species karyotyped), namely as Baryancistrus, Corumbataia, Farlowella, Harttia, Hisonotus, Lasiancistrus, Loricaria, Loricariichthys, Neoplecostomus, Panaqolus, Panaque, Pareiorhina, Pseudacanthicus, Pterygoplichthys, and Scobinancistrus. On other hand, the multiple distribution of Ag-NOR seems to be conserved only in Hypancistrus, while other genus as Ancistrus, Hypostomus, and Rineloricaria present both simple and multiple distributions on chromosomes.
Although distributed throughout the Neotropical region, there is a predominance of cytogenetic studies in Loricariidae species from Brazil (Fig. 2). Few studies were conducted in other countries that includes Argentina, Ecuador, Paraguay, and Venezuela. Notably, those in Argentina and Paraguay were mostly restricted to the frontier region with Brazil. When accounting the Brazilian territory, is also notable that some regions are poorly represented in cytogenetic studies, especially the northeast in which at least nine states have not been included in the cytogenetic samplings. In addition, the Guianas Shield and Western Amazon regions are largely recognized as neglected regions in biogeographical and evolutionary studies (Cassemiro et al., 2023), also with little or absent cytogenetic information for Loricariidae. Despite the regional sampling gap problem, Loricariidae diversity is still insufficiently represented by cytogenetic studies. Our compilation recorded 234 species assessed by cytogenetic studies, that in comparison to the 1,051 valid species (Fricke et al., 2023), represents 22.26% of the family species richness. The diversity of genus assessed by cytogenetic studies was the highest in Hypoptopomatinae (42.1%), followed by Rhinelepinae (28.5%), Hypostominae (27.2%), Loricariinae (24.4%), Delturinae (20%), and Lithogeninae (0%). Besides Lithogeninae that do not have any species karyotyped to date, the subfamily Delturinae has only one genus and two unidentified species karyotyped: Hemipsilichthys sp. Paraitinga River (Kavalco et al., 2004, 2005), and Hemipsilichthys n. sp. Patos River (Alves et al., 2005). We suggest that further cytogenetic studies focus on expand the sampling in the northeast Brazil, the Western Amazon, the Guianas Shield, and other Neotropical countries, in addition to evaluate a more representative portion of the diversity.
ACKNOWLEDGEMENTS
The authors are grateful to all cytogeneticists who contributed to the increase of the knowledge about Loricariidae cytogenetics. We also thank to the Fundação de Amparo à Pesquisa do Estado de São Paulo (FMCS 2020/02681–9, 2022/04261–2, and 2023/08116–0; MBC AR-23/00955–2), to Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPQ (MBC 302928/2021–9), and Instituto Nacional de Ciência e Tecnologia da Biodiversidade e uso Sustentável de Peixes Neotropicais – INCT Peixes (405706/2022–7).
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ADDITIONAL NOTES
Publication Dates
-
Publication in this collection
10 Jan 2025 -
Date of issue
2024
History
-
Received
06 Jan 2024 -
Accepted
28 Oct 2024
