Are the chromosomal fusions that shaped the karyotype of Tetranematichthys wallacei (Siluriformes: Auchenipteridae) a shared feature among Ageneiosini species?

Abstract

The genus Tetranematichthys has only three species, and none of them have undergone cytogenetic analyses. Therefore, this study brings for the first time the analysis of Tetranematichthys wallacei, collected from the Igarapé Apaú, Guamá River basin, municipality of Castanhal, Pará State, Brazil. The diploid number found was 52 chromosomes (32m+18sm+2st, NF = 104), in both sexes, with predominantly terminal and some interstitial heterochromatin. Telomeric sequences were observed exclusively in terminal regions. The 18S rDNA sites were found on pair 17sm of all specimens and in only one of the homologous of pair 7 in three specimens. The 5S rDNA sites were found in pairs 8m and 10m. Tetranematichthys wallacei exhibits characteristics worthy of attention regarding its current phylogenetic position, including a probable diploid number reduction. Additionally, it shares with Tympanopleura atronasus the 18S rDNA allocated in the long arm of a large sm chromosome (first pair) but does not share with Ageneiosus the large first m pair with evidence of fusion, as observed in Ageneiosus inermis. The chromosomal data generated for T. wallacei, along with the data from the other two previously studied Ageneiosini taxa, reinforces proposals from morphology-based studies suggesting that the tribe represents the most distinct clade within the family.

Keywords:
Chromosomal evolution; Driftwood catfish; Diploid number reduction; Interstitial telomeric sites; rDNA polymorphism

Resumo

O gênero Tetranematichthys possui apenas três espécies, e nenhuma delas tinha sido submetida a análises citogenéticas. Assim, este estudo traz pela primeira vez a análise de Tetranematichthyswallacei, coletado no Igarapé Apaú, bacia do rio Guamá, cidade de Castanhal, estado do Pará, Brasil. O número diploide de 52 cromossomos (32m+18sm+2st, NF = 104) foi encontrado em ambos os sexos, com heterocromatina predominantemente terminal e algumas intersticiais. A sequência telomérica foi observada exclusivamente em regiões terminais. Os sítios de 18S rDNA foram encontrados no par 17sm de todos os exemplares e em apenas um dos homólogos do par 7 em três exemplares. Os sítios de 5S rDNA foram encontrados nos pares 8m e 10m. Tetranematichthyswallacei possui algumas características que dignas de quanto à sua posição filogenética atual, incluindo uma provável redução no número diploide. Além disso, T.wallacei compartilha com Tympanopleuraatronasus o 18S rDNA alocado no braço longo de um grande cromossomo sm (primeiro par), mas não compartilha com Ageneiosus o primeiro par m grande com evidências de fusão, como observado em Ageneiosus inermis. Os dados cromossômicos gerados para T. wallacei, juntamente com os dados dos outros dois táxons de Ageneiosini estudados anteriormente, reforçam propostas de estudos baseados em morfologia que sugerem que a tribo representa o clado mais diferenciado dentro da família.

Palavras chave:
Bagres de troncos; Evolução cromossômica; Polimorfismo de DNAr; Redução do número diploide; Sítios teloméricos intersticiais

INTRODUCTION

The Neotropical region extends from Mexico to Argentina and the Caribbean (Morrone, 2014), with an unparalleled representation in terms of fish biodiversity (Reis et al., 2016). The Auchenipteridae family comprises 128 valid species distributed across 25 genera (Fricke et al., 2024). Ageneiosus Lacepède, 1803 and Tetranematichthys Bleeker, 1858 belong to the tribe Ageneiosini within Auchenipterinae and have a closely linked taxonomic history, being considered sister groups (e.g., Bleeker, 1862; Miranda Ribeiro, 1911; Britski, 1972; Ferraris, 1988; Royero, 1999; Birindelli, 2014). These genera are so closely related that the first species of Tetranematichthys was initially described and classified within Ageneiosus (Ageneiosusquadrifilis; Walsh et al., 2015). Only a few years later, this species was reclassified as Tetranematichthys quadrifilis (Kner, 1858), leading to the establishment of the genus Tetranematichthys (Vari, Ferraris, 2006). Recently, Calegari et al.(2019) carried out research based on both morphological and molecular data in Auchenipteridae and concluded that Tetranematichthys and Ageneiosus share sufficient similarities, from both phylogenetic and historical perspectives, to be considered monophyletic sister clades.

Cytogenetic studies are increasingly valuable tools for exploring biodiversity in diverse fish groups (Cioffi, Bertollo, 2012; Ditcharoen et al., 2019). Classical characterization and banding techniques, combined with chromosomal mapping of repetitive DNA sequences, have become important to understand karyotypic congruences and divergences (Bertollo et al., 2017). It can demonstrate characters that are usually not accessible by other research methods, contributing to the visualization of possible evolutionary paths in distinct groups of fish due to their specific chromosomal and genomic characteristics (Cioffi et al., 2018; Ditcharoen et al., 2019). One of the best well-known examples of the importance of cytogenetic analyses is the Wolf Fish Hoplias malabaricus (Bloch, 1794) (Characiformes, Erythrinidae). Although very similar morphologically, this is a species complex composed of seven major karyomorphs (A-G), which is possibly reproductively isolated and has been mainly diagnosed through cytogenetic methods (reviewed in Cioffi et al., 2018). Another noteworthy example is Astyanax scabripinnis (Jenyns, 1842), which was initially composed of six populations from different Brazilian watersheds. However, cytogenetic studies were pioneering in demonstrating a great hidden biodiversity within this taxon, which is currently recognized as a species complex with more than 30 species (reviewed in Cioffi et al., 2018). Other important examples can also be found in less-known Neotropical fish groups. For instance, within Auchenipteridae, a species complex is suggested for Trachelyopterus galeatus (Linnaeus, 1766) (Siluriformes: Auchenipteridae, Santos et al., 2021). Cytogenetic data was also crucial to identify hidden diversity within Ancistrus Kner, 1854 (Siluriformes, Loriicaridae) from the Paraná River basin (Prizon et al., 2017), and it was used to suggest the reallocation of genera in Hypostomini catfishes (Siluriformes, Anjos et al., 2019).

However, out of the 25 currently valid genera in Auchenipteridae, chromosomal data are available for only eight genera: Ageneiosus, Auchenipterus Valenciennes, 1840, Centromochlus Kner, 1858, Entomocorus Eigenmann, 1917, Glanidium Lütken, 1874, Trachelyopterus Valenciennes, 1840, Tatia Miranda Ribeiro, 1911, and Tympanopleura Eigenmann, 1912 (Tab. 1). Notably, within the Ageneiosini tribe, cytogenetic investigations have been conducted only on Ageneiosus and Tympanopleura, with Tetranematichthys remaining unstudied. Tetranematichthys represents one of the earliest divergent lineages within Ageneiosini and is regarded as the sister group of Ageneiosus + Tympanopleura (Calegari et al., 2019). Therefore, the chromosomal characterization of Tetranematichthys species is essential for a more comprehensive understanding of the chromosomal evolutionary trajectory within Ageneiosini, including potential apomorphic and plesiomorphic conditions. Tetranematichthys currently comprises three species: T.barthemi Peixoto & Wosiacki, 2010, T.quadrifilis, T.wallacei Vari & Ferraris, 2006. This paper presents the first chromosomal analysis of a Tetranematichthys species: Tetranematichthys wallacei.

TABLE 1 |
An overview of cytogenetic data in Auchenipteridae. 2n: diploid number; FN: fundamental number; SS: sex chromosome system; m: metacentric; sm: submetacentric; st: subtelocentric; a: acrocentric; p: short arm; q: long arm; i: interstitial; t: terminal. CA: chromosome arm; PCA: position on the chromosome arm; CM: chromosome morphology; CITS: chromosome with interstitial telomere sequence; NI: ITS not investigated; ND: ITS not detected; Ref: References. AM: Amazonas; GO: Goiás; PA: Pará; PR: Paraná; MT: Mato Grosso; MG: Minas Gerais; MS: Mato Grosso do Sul; RN: Rio Grande do Norte. References: 1. Fenocchio, Bertollo (1992); 2. Lui et al. (2013a); 3. Present study; 4. Ravedutti, Júlio (2001); 5. Machado et al. (2021); 6. Santos et al. (2021); 7. Haerter et al. (2022); 8. Lui et al. (2021); 9. Lui et al. (2010); 10. Araújo, Molina (2013); 11. Fenocchio et al. (2008); 12. Lui et al. (2015); 13. Lui et al. (2013b); 14. Kowalski et al. (2020); 15. Kowalski et al. (2024); 16. Haerter et al. (2023); 17. Felicetti et al. (2023); 18. Felicetti et al. (2021); *species cited with a name different from that currently valid.

Auchenipterinae
Ageneiosini
Ageneiosus inermis (*cited as Ageneiosus brevifilis)	Solimões River, Manaus (AM), Brazil	56	102	-	20	16	10	10		p	t	sm	-	-	-	-	NI	1*
	Araguaia River, Aragarças (GO), Brazil	56	108	-	32	16	4	4	20	p	t	sm	4	p		m	pair 1m, p	2
Tympanopleura atronasus (cited as Ageneiosus atronasus)	Solimões River, Manaus (AM), Brazil	56	100	-	16	16	12	12	-	q	i	sm	-	-	-	-	NI	1
Tetranematichthys wallacei	Guamá River (PA), Brazil	52	104	-	32	18	2	-	17	q	t	sm	8	p	t	m	ND	3
													10	p	t	m
Auchenipterini
Auchenipterus nuchalis	Araguaia River, Aragarças (GO), Brazil	58	110	-	22	16	14	6	14	p	t	sm	22	p	t	st	NI	5
Auchenipterus osteomystax (cited as Auchenipterus nuchalis)	Paraná River, Porto Rico (PR), Brazil	58	106	-	24	14	10	10	15	p	i	sm	-	-	-	-	NI	4
Entomocorus radiosus	Paraguai River, Poconé (MT), Brazil	58	106	-	22	12	14	10	21	p	t	st	12	p	t	sm	NI	5
													13	p	t	sm
													14	p	t	sm
													15	p	t	sm
													16	p	t	sm
													18	p	t	st
													19	p	t	st
Trachelyopterini
Trachelyopterus coriaceus	Araguaia, São Miguel do Araguaia (GO), Brazil	58	108	-	20	18	12	8	23	p	t	st	3	p	t	m	NI	6,7, 16
													16	q	i	sm
Trachelyopterus aff. coriaceus (*cited as Trachelyopterus sp.)	Bento Gomes, Poconé (MT), Brazil	58	108	-	22	20	8	8	22	p	t	st	16	p	i	sm	ND	8*, 16
													18	q	t	sm
Trachelyopterus galeatus (*cited as Parauchenipterus galeatus)	Amazonas River, Catalão Lake, Manaus (AM), Brazil	58	106	-	20	12	18	8	20	p	t	sm	14	p	t	sm	ND	7, 16 17, 18
													17	q	t	sm
	Paraná River, Paraná River basin (MS), Brazil	58	108	-	24	18	8	8	25	p	t	sm	16	p	i	sm	NI	9*
													17	q	i	sm
	Piumhi River, Paraná River basin (MG), Brazil	58	108	-	20	16	14	8	24	p	t	st	15	p	i	sm	NI	9*
													16	q	i	sm
	Lagoa da Prata, São Francisco River basin (MG), Brazil	58	108	-	22	16	12	8	23	p	t	st	16	p	i	sm	ND	9*
													17	q	i	sm
	Pium River, Paranamirim (RN), Brazil	58	108	-	24	16	10	8	-	p	-	sm	-	-	-	-	NI	10*
	Paraná River, Porto Rico (PR), Brazil	58	98		22	12	6	18	23	p	t	a	-	-	-	-	NI	4*
	Araguaia River, São Miguel do Araguaia (GO), Brazil	58	108	-	20	18	12	8	24	p	t	sm	3	p	t	m	NI	6*, 7, 16
	Miranda River, Paraguay River basin (PY), Brazil	58	108	-	24	12	14	8	24	p	t	st	14	p	t	sm	ND	17, 18
													17	q	i	sm	ND
Trachelyopterus porosus	Catalão Lake, Amazonas River basin (AM), Brazil	58	106	-	22	16	10	10	23	p	-	st	3	p	i	m	ND	7, 16, 17, 18
													4	p	t	m
	Miranda River, Paraguay River basin (MS), Brazil	58	106	-	22	16	10	10	23	p	t	st	3	p	i	m	ND	17
													4	p	t	m
Trachelyopterus striatulus (*cited as Parauchenipterus striatulus)	Doce River basin, Mariléia (MG), Brazil	58	106	-	18	20	10	10	23	p	t	st	10	p	i	sm	NI	6*, 16
													13	p	i	sm
													15	q	i	sm
Centromochlinae
Glanidiini
Glanidium ribeiroi	Iguaçu River, Reservoir Salto Caxias (PR), Brazil	58	112	-	28	16	10	4	17	p	i	sm	-	-	-	-	NI	4
	Iguaçu River, Reservoir Segredo (PR), Brazil	58	106	-	22	16	10	10	13	p	i	sm	-	-	-	-	NI	11
	Iguaçu River, Reservoir Salto Osório (PR), Brazil	58	106	-	22	16	10	10	13	p	i	sm	-	-	-	-	NI	11
	Iguaçu River, Capanema (PR), Brazil	58	110	-	22	20	10	6	14	p	i	sm	16	q	i	sm	ND	12
Tatia jaracatia	Iguaçu River, Capanema (PR), Brazil	58	116	-	20	26	12	-	28	p	t	st	4	p	i	m	NI	13
													18	p	t	sm
													19	q	i	sm
													29	p	t	st
Tatia neivai	Machado River, Denise (MT), Brazil	58	116	-	26	26	6	-	28	p	t	st	4	p	i	m	NI	13
													21	p	t	sm
													22	q	i	sm
Centromochlini
Centromochlus heckelii	Solimões River, Manaus (AM), Brazil	46	72	♂ ZZ	14	6	6	20	20	p	t	a	-				NI	14
									ZZ	p	p	st
				♀ ZW	15	6	5	20	20	p	p	a
									ZW	p	t	st/m
Centromochlus schultzi	Xingu River basin, Altamira (PA), Brazil	58	108	-	26	16	8	8	24	p	i	st	4	p	i	m	pair 1m, p pair 3m, c	15
													24	p	i	st
													27	p	t	a
													28	p	t	a

MATERIAL AND METHODS

In this study, 11 individuals (3 females and 8 males) of T. wallacei were collected from the Igarapé Apaú, Guamá River basin, 01°23’20.5”S 47°59’07.4”W, in municipality of Castanhal, Pará State, Brazil (Fig. 1). The mitotic chromosomes were obtained from anterior kidney cells according to Bertollo et al.(2015). The animals were euthanized by an overdose of clove oil (Griffiths, 2000) and deposited at the ichthyology collection of the Universidade Tecnológica Federal do Paraná, Santa Helena (Voucher ID CISH 861). Chromosomal morphology was determined following the protocol outlined by Levan et al.(1964). The fundamental number (NF) was calculated considering metacentric (m), submetacentric (sm) and subtelocentric (st) chromosomes as having 2 arms, and acrocentric (a) as having only 1 arm. Nucleolus organizing regions (AgNORs) were visualized through silver nitrate impregnation (Howell, Black, 1980) and heterochromatin distribution was determined according to the C-band technique described by Sumner (1972), with modifications in staining step as proposed by Lui et al.(2012).

Fluorescent in situ hybridization (FISH) was performed according to Pinkel et al.(1986), with modifications suggested by Margarido, Moreira-Filho (2008). A stringency of 77% was applied for the 18S and 5S rDNA probes (200ng of each probe, 50% deionized formamide, 10% dextran sulfate, 2x SSC, at 37 ºC overnight). Similarly, fluorescent in situ hybridizations with telomeric probes were initially performed using 77% of stringency. However, due to a probable diploid number reduction in this species, FISHs were also carried out at 62% stringency to identify potential degenerated ITSs. The 5S rDNA and 18S rDNA probes were obtained from minipreps of Megaleporinus elongatus (Valenciennes, 1850) (Martins, Galetti Jr., 1999) and Prochilodus argenteus Spix & Agassiz, 1829 (Hatanaka, Galetti, 2004), respectively. They were labeled with Digoxigenin-11-dUTP (Dig-Nick-Translation Mix, Roche, according to the manufacturer’s instructions) and detected using Anti-Digoxigenin-Rhodamine or labeled with Biotin-16-dUTP (Bio-Nick-Translation Mix, Roche, according to the manufacturer’s instructions) and detected with Streptavidin-FITC (Roche).

FIGURE 1 |
Map showing the sampling location of Tetranematichthys wallacei from the Guamá River basin. Geographical data source: Instituto Brasileiro de Geografia e Estatística (IBGE). Datum: SIRGAS 2000.

The telomeric probes were generated and labeled by PCR reaction using the primers described by Ijdo et al. (1991) with the following specifications: 1x buffer, 25 mM MgCl2, 0.2 mM dNTPs, 1 µM of each primer, 0.5 U of Taq DNA polymerase (Roche) and 0.025 mM Tetramethyl-Rhodamine-5-dUTP (Roche). The PCR conditions were: 95°C (1 min), 10 cycles of 95°C (1 min), 55°C (30 s) and 72°C (1 min); of 30 cycles of 95°C (1 min), 60°C (30 s) 72°C (30 s), and final extension at 72°C (1 min). Digital images were captured using the DP Controller 3.2.1.276 software with an Olympus DP71 digital camera connected to a BX61 epifluorescence microscope (Olympus America Inc., Center Valley, PA, United States of America).

RESULTS

The diploid number observed for T. wallacei was 2n = 52 chromosomes (32m + 18sm + 2st, NF = 104), with no differences between the sexes (Fig. 2A). Most heterochromatic blocks appeared pale and were located at the terminal regions; however, some pericentromeric blocks were also observed in pairs 2m, 6m, and 17sm, and centromeric blocks were evident in pairs 1m, 4m, 5m, 18sm, and 20sm (Fig. 2B). Fluorescent in situ hybridization (FISH) with 18S rDNA probes revealed markings at the terminal positions on the long arm of pair 17sm in all analyzed specimens (Fig. 3A). Additionally, three individuals (two males and one female) exhibited an additional 18S rDNA site on a single chromosome of pair 7m, located at the terminal position of its short arm (Fig. 3A, in box). No specimen in our sample exhibited two pairs completely marked (four chromosomes) with the 18S rDNA probes. The AgNORs were coincident with the 18S rDNA sites on pair 17 (Fig. 2A, in box). FISHs with 5S rDNA probes showed this cistron is located at the proximal position of the short arm at the pairs 8m and 10m (Fig. 3A). FISH with the telomeric sequence (TTAGGG)n revealed markings exclusively at the terminal regions, with no presence of interstitial telomeric sites (ITS) (Fig. 3B).

FIGURE 2 |
A. Karyotype of Tetranematichthys wallacei Stained with Giemsa; and B. Karyotype of T. wallacei sequentially submitted to C-banding. AgNORs presented in the box. Scale bar = 10 µm.

FIGURE 3 |
A. Karyotype of Tetranematichthys wallacei hybridized with 18S rDNA (green signal in pair 17) and 5S rDNA (red signal in pairs 8 and 10) probes, counterstained with DAPI. The 18S rDNA polymorphism, represented by an additional chromosome carrying the 18S rDNA sites (pair 7) are presented in the box. B. Methaphase plate of T. wallacei hybridized with telomeric probes under 77% of stringency. Scale bars = 10 µm.

DISCUSSION

Doradidae and Auchenipteridae are the only families within the superfamily Doradoidea, a monophyletic clade supported by several morphological and molecular data (Birindelli, 2014; Calegari et al., 2019). The cytogenetic studies on most Auchenipteridae species have revealed a diploid number (2n) of 58 chromosomes (Tab. 1). This 2n is also prevalent in the sister group Doradidae (Takagui et al., 2021), which may suggest that it represents the plesiomorphic condition for both families, as indicated by other studies (Baumgärtner et al., 2016; Kowalski et al., 2020; Machado et al., 2021). However, the reconstruction of the basal diploid number (2n) in Doradidae provided limited support for the 58 chromosomes as the plesiomorphic condition, as it was equally parsimonious as the 2n = 56 (Takagui et al., 2021). The low support values in this case may be attributed to the small number of species karyotyped so far, a challenge that also affects Auchenipteridae. This makes the karyotypic description of new species, such as T. wallacei, even more important to reconstruct the ancestral 2n for Auchenipteridae and Doradoidea.

Although Takagui et al.(2021) had focused only on Doradidae, such data also introduces uncertainty about the 2n = 58 being the plesiomorphic condition in Auchenipteridae. Thus, also considering the diploid numbers of 56 and 58 chromosomes as potential plesiomorphic conditions for Auchenipteridae, the 2n = 52 chromosomes in T. wallacei indicates a diploid number reduction. In addition, the diploid number reduction in other members of Ageneiosini, including Ageneiosus inermis (Linnaeus, 1766) (cited as Ageneiosus brevifilis, Fenocchio, Bertollo, 1992; Lui et al., 2013a) and Tympanopleura atronasus (Eigenmann & Eigenmann, 1888) (Fenocchio, Bertollo, 1992) with 56 chromosomes, indicates that the reduction of the 2n can be a shared feature among the species of this tribe.

While most Auchenipteridae species exhibit a 2n = 58 (Tab. 1), various diploid numbers have been observed within the family. For instance, A. inermis (cited as A. brevifilis, Fenocchio, Bertollo, 1992; Lui et al., 2013a) and T. atronasus(Fenocchio, Bertollo, 1992) with 56 chromosomes, and Centromochlus heckelii (De Filippi, 1853) (Kowalski et al., 2020) with 46 chromosomes. Considering that A. inermis, T. atronasus and T. wallacei belong to Auchenipterinae, and C. heckelii to Centromochlinae, which is strongly supported by an extensive database and previous research (e.g., Ferraris, 2007; Birindelli, 2014; Calegari et al., 2019), it is evident that these lower diploid numbers (56 and 52 in Auchenipterinae-Ageneiosini versus 46 in Centromochlinae) result from independent evolutionary processes. Although it might be intuitive to attribute these lower diploid numbers in Auchenipteridae (56, 52 and 46) to chromosomal fusion events, as suggested by some studies (Lui et al., 2013a; Kowalski et al., 2020), ITS (Interstitial Telomeric Sequence) sites have been detected only in A. inermis from the Araguaia River basin (Lui et al., 2013a).

Telomeres consist in noncoding TTAGGG repeats and associated proteins that protect chromosome ends from degradation, aberrant recombination, and end-to-end fusion (Hartmann et al., 2004). The absence or inactivation of this structure/sequence allows the chromosomal end fusion. In some groups of vertebrates these chromosomal fusions occur without several loss of telomeric sequence, resulting in interstitial telomeric sites (Meyne et al., 1989, 1990; Slijepcevic, 1998), whose detection by FISH is considered a strong indicator of a fusion point by some researchers (e.g., Rosa et al., 2012; Lui et al., 2013a; Deon et al., 2020). Tetranematichthys wallacei have not presented ITS under 77% (Fig. 3B) or 62% of stringency (data not shown, same result as 77%). However, it is worth noting that there are species with no ITS even though fusion events were suggested to explain a 2n reduction, as in the case of Heptapterus hollandi (Haseman, 1911), which presented the lowest diploid number at that time in Heptapteridae (Margarido, Moreira-Filho, 2008). Therefore, the absence of ITSs in T. wallacei does not necessarily mean that chromosomal fusions have not occurred.

In Auchenipteridae, heterochromatin is typically pale and located at the terminal regions of the chromosomes (e.g., Lui et al., 2010, 2013a,b, 2015; Kowalski et al., 2020; Machado et al., 2021; Santos et al., 2021). However, heterochromatic blocks in centromeric, pericentromeric or interstitial position have been reported in some species (e.g., Lui et al., 2013a,b; Kowalski et al., 2020; Machado et al., 2021). In addition to the terminal heterochromatin commonly found in Auchenipteridae, T. wallacei also exhibited chromosomes with centromeric and pericentromeric heterochromatic blocks (Fig. 2B). In other Ageneiosini species, only the pair 1m of A. inermis from the Araguaia River basin has shown pericentromeric heterochromatin, which coincided with the ITS found in this population (Lui et al., 2013a).

In Ageneiosini, C-banding techniques were performed on three species: A. inermis from the Araguaia River (Lui et al., 2013a) and the Solimões River (Fenocchio, Bertollo, 1992), and T. atronasus (Fenocchio, Bertollo, 1992). However, the organization of the chromosomes into a karyotype was only performed in A. inermis from the Araguaia River (Lui et al., 2013a). In the other species, only the metaphases were presented, and in T. atronasus, the C-banding was presented only for the pair carrying the NORs (Fenocchio, Bertollo, 1992). This scarcity of non-terminal heterochromatins in Ageneiosus (except for the first m chromosome pair) and their absence in Tympanopleura species analyzed so far, allows us to suggest that the non-terminal blocks detected in T. wallacei might correspond to chromosomal fusion sites. There are several reports of species from different groups of fish presenting co-located ITS and heterochromatin, such as Trachydoras paraguayensis (Eigenmann & Ward, 1907) (Baumgärtner et al., 2016), Harttia sp. 2 (Deon et al., 2020), Rineloricaria lima (Kner, 1853) (Rosa et al., 2012) and Corydoras lacrimostigmata Tencatt, Britto & Pavanelli, 2014 (Barbosa et al., 2017).

Regarding the proposal by Lui et al. (2013a) that the chromosomal fusion detected in A. inermis could be a basal event among the Ageneiosus, our data make it possible to expand this hypothesis. At the time of the publication by Lui et al.(2013a), only Ageneiosus and Tetranematichthys had been included in Ageneiosini. However, Walsh et al.(2015) later revalidated Tympanopleura, which was composed by a fraction of the species previously allocated in Ageneiosus. According to this new scenario, it is possible to assume that the fusion event reported by Lui et al.(2013a) can constitute a basal event before the cladogenesis of Ageneiosus and Tympanopleura.

The first m chromosome pair, visibly larger in size than the others, seems to be shared between the Ageneiosini species (Lui et al.,2013; Fenocchio, Bertollo, 1992). This same chromosome pair was suggested to have originated through a fusion event in A. inermis due to the presence of an ITSat the proximal region of the short arm (Lui et al.,2013a). While Tetranematichthys is considered sister group of Ageneiosus (Birindelli, 2014; Calegari et al., 2019), it was not possible to distinguish any chromosomal pair that could represent this chromosome pair in T. wallacei (Figs. 2–4). Two hypothesis can be proposed to explain this chromosomal arrangement: (1) the basal fusion proposed by Lui et al.(2013a) occurred before the diversification of the clade that gave rise to the species of Ageneiosus and Tympanopleura, and consequently, after the cladogenesis that originated Tetranematichthys; or (2) the fusion occurred at the clade base of all Ageneiosini and had underwent subsequent rearrangements in the Tetranematichthys lineage, reducing its size compared to its probable counterpart chromosome, the large chromosome pair present in Ageneiosus and Tympanopleura species.

In Ageneiosini, despite the limited cytogenetic data, the first m chromosome pair is not the only chromosomal pair that stands out due to its size. The first submetacentric pair detected in T. atronasus and T. wallacei is notably similar as well, suggesting that T. atronasus and T. wallacei also share a common characteristic, which has not been identified in Ageneiosus species yet (Fig. 4). Considering the phylogenetic proposals for the group, it seems that Ageneiosus might have lost this character during its karyotypic evolution. On the other hand, and considering this first sm pair shared between Tetranematichthys and Tympanopleura, the following question may emerge: could the phylogenetic relationships among the three Ageneiosini genera be different? This issue becomes even more interesting if we remember that this sm chromosome pair is the 18S rDNA carrier in T. atronasus and T. wallacei.

Several characteristics regarding the distribution of 18S rDNA sites in Auchenipteridae are worth highlighting: (1) in most species the 18S rDNA has been found at terminal position of st or a chromosome pairs, and less frequently at sm pairs and interstitial positions (Tab. 1); (2) except for T. atronasus and T. wallacei, all the species exhibit the 18S rDNA at the short arm (Tab. 1); (3) except for T. atronasus and T. wallacei, all the species exhibit 18S rDNA at chromosome pairs with medium or small size compared to the other chromosomes into its respective karyotype (Tab. 1; Figs. 2, 4). The unique characteristic of the first sm chromosome pair bearing the 18S rDNA on the long arm further distinguishes T. atronasus and T. wallacei from other karyotyped Auchenipteridae species. The noticeably larger size of this chromosome pair also contributes to this distinction. This raises the possibility of a homoplastic character, particularly in light of the most recent phylogenetic proposal for the Ageneiosini, which consider Tetranematichthys as the sister group of Ageneiosus + Tympanopleura. Future research on other Ageneiosini species will be crucial to expand this discussion. Currently, only three species out of the 21 in the tribe (Fricke et al., 2024) have been cytogenetically studied, with T. wallacei being the most recent addition.

FIGURE 4 |
Idiogram representing the karyotypes of Ageneiosus inermis (adapted from Fenocchio, Bertollo, 1992; Lui et al., 2013a), Tympanopleura atronasus (adapted from Fenocchio, Bertollo, 1992) and Tetranematichthys wallacei (present study).

In T. atronasus and T. wallacei, the 18S rDNA has been observed on the long arm of the first submetacentric pair, but their positions differ, being proximal and terminal, respectively (Tab. 1; Fig. 4). Among Auchenipteridae, only Glanidium ribeiroi Haseman, 1911 (Ravedutti, Júlio, 2001; Fenocchio et al., 2008; Lui et al., 2015) and Auchenipterus osteomystax Miranda Ribeiro, 1918 (cit. Auchenipterus nuchalis, Ravedutti, Júlio, 2001) exhibited NORs located in interstitial chromosomal regions (Tab. 1). Usually, the occurrence of interstitial NORs for some species within groups with a history of terminal position, such as Auchenipteridae and Doradidae, have been attributed to pericentric and/or paracentric inversion occurrence (Ravedutti, Júlio, 2001; Eler et al., 2007; Milhomem et al., 2008; Takagui et al., 2022). Therefore, the variation in the position 18S rDNA in this sm chromosome pair shared between T. wallacei and T. atronasus might also be attributed to a paracentric inversion.

In addition to pair 17sm, three specimens (two males and one female) showed 18S rDNA probe signals at the terminal position of the short arm of a single chromosome from pair 7m, indicating an intrapopulation chromosomal polymorphism. Another noteworthy observation is that T. wallacei and C. heckelii are the only Auchenipteridae species with multiple 18S rDNA sites, and this marks the first report of a polymorphism involving the 18S rDNA in the family. Since there is no similar description in Auchenipteridae, it is worth noting the observation in Anadoras grypus (Cope, 1872), from the sister group Doradidae, which also had up to three chromosomes bearing the 18S rDNA and similar variations in the position of the rDNA sequence as those found in T. wallacei(Takagui et al.,2022). Among the different possible chromosomal rearrangements, the remnant of a non-reciprocal translocation event is pointed as the hypothesis to explain the origin of the polymorphism found in Anadoras grypus (Takagui et al.,2022), and from a second pair bearing 18S rDNA in C. heckelii(Kowalski et al.,2020). Likewise, a transposition event could be responsible for the dissemination of this sequence in T. wallacei.

In contrast to the 18S rDNA, which shows a more varied distribution, the 5S rDNA has been identified in various chromosomes and positions across Auchenipteridae (Machado et al., 2021; Santos et al., 2021; Haerter et al., 2022). In Ageneiosini, only one population had been analyzed with this marker, A. inermis (Lui et al., 2013a). When compared to T. wallacei, it is notable that the 5S rDNA was found on chromosomes with the same morphology (metacentric) and on short arms of both species. Given the similarity in chromosomal morphology and the location of the 5S rDNA site, one of the chromosomal pairs found in T. wallacei may correspond to pair 4m in A. inermis (Lui et al.,2013a). The 5S rDNA exhibits high diversity in Auchenipteridae, presenting both simple and multiple sites (Tab. 1), a barrier to the establishment of a plesiomorphic condition. Hence, two hypothetical scenarios can be considered for the chromosomal evolution of this marker in Ageneiosini: (1) if the plesiomorphic condition entails only one chromosome carrying the 5S rDNA sites, the second pair of T. wallacei may have been originated from a transposition event; or (2) if the ancestral condition involves multiple sites, A. inermis may have lost 5S rDNA sites during its evolutionary trajectory.

In addition to the potential transposition events involving ribosomal sequences in T. wallacei, it is important to consider the organization of mitotic chromosomes during interphase. Chromosomes are arranged into specific chromosomal territories to maintain their individuality throughout the cell cycle, positioning adjacent to each metaphase phase, a concept known as the “Rabl Model” (Cremer et al., 1982, 2018; Cremer, Cremer, 2010). This arrangement facilitates spatial organization in a paired manner, enhancing the proximity and/or contact between chromosomes, thereby enabling the potential transfer of genetic material in the same position between adjacent chromosomes (Cremer et al., 1982, 2010, 2018), including rDNAs, as previously suggested for other Auchenipteridae species (e.g., Kowalski et al., 2020; Machado et al., 2021).

Tetranematichthyswallacei exhibits some characteristics that stand out: (1) a diploid number reduction unprecedented for Auchenipteridae; (2) it shares with T. atronasus the 18S rDNA in the long arm of a submetacentric chromosome, which have not been reported in Auchenipteridae yet; (3) first submetacentric pair possibly shared with T. atronasus and, thus far, exclusive to Ageneiosini. Some studies (Regan, 1911; Miranda Ribeiro, 1911; Eigenmann, 1925; Fowler, 1951; Greenwood et al., 1966; among others) suggested the members of Ageneiosini should be allocated into an exclusive clade, the Ageneiosidae. However, with the advancement of analyses involving new tools and more samples, this classification proved to be unsustainable, and recent data based on morphological and molecular characters by Calegari et al.(2019) definitively ruled out this possibility. Although there is no doubt about the species in this group being part of Ageneiosini, it is important to highlight that this tribe seems to be markedly different from other Auchenipteridae.

ACKNOWLEDGEMENTS

We thank Dr. José L. O. Birindelli (MZUEL) and Heleno Brandão (CISH) for the identification of the specimens; the fishermen José Pedro Silva Duarte and Minoru Hoshi for their assistance in sampling; Instituto Chico Mendes de Conservação da Biodiversidade for authorizing the collection of the specimens. This study was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and Fundação Araucária de Apoio ao Desenvolvimento Científico e Tecnológico do Estado do Paraná (FA).

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ADDITIONAL NOTES

• HOW TO CITE THIS ARTICLE

  Casarotto CC, Haerter CAG, Perin DP, Jesus LM, Antoniazzi GJ, Blanco DR, Treco FR, Margarido VP, Traldi JB, Lui RL. Are the chromosomal fusions that shaped the karyotype of Tetranematichthys wallacei (Siluriformes: Auchenipteridae) a shared feature among Ageneiosini species? Neotrop Ichthyol. 2024; 22(2):e240015. https://doi.org/10.1590/1982-0224-2024-0015

Edited-by

George Mattox

Publication Dates

• Publication in this collection
  22 July 2024
• Date of issue
  2024

History

• Received
  17 Feb 2024
• Accepted
  21 May 2024