Deciphering the Evolutionary History of Arowana Fishes (Teleostei, Osteoglossiformes, Osteoglossidae): Insight from Comparative Cytogenomics

Abstract

Arowanas (Osteoglossinae) are charismatic freshwater fishes with six species and two genera (Osteoglossum and Scleropages) distributed in South America, Asia, and Australia. In an attempt to provide a better assessment of the processes shaping their evolution, we employed a set of cytogenetic and genomic approaches, including i) molecular cytogenetic analyses using C- and CMA3/DAPI staining, repetitive DNA mapping, comparative genomic hybridization (CGH), and Zoo-FISH, along with ii) the genotypic analyses of single nucleotide polymorphisms (SNPs) generated by diversity array technology sequencing (DArTseq). We observed diploid chromosome numbers of 2n = 56 and 54 in O. bicirrhosum and O. ferreirai, respectively, and 2n = 50 in S. formosus, while S. jardinii and S. leichardti presented 2n = 48 and 44, respectively. A time-calibrated phylogenetic tree revealed that Osteoglossum and Scleropages divergence occurred approximately 50 million years ago (MYA), at the time of the final separation of Australia and South America (with Antarctica). Asian S. formosus and Australian Scleropages diverged about 35.5 MYA, substantially after the latest terrestrial connection between Australia and Southeast Asia through the Indian plate movement. Our combined data provided a comprehensive perspective of the cytogenomic diversity and evolution of arowana species on a timescale.

African Arowana Genome Provides Insights on Ancient Teleost Evolution

“…The divergence time of each internal node was calculated using MCMCTree ( Yang, 2007 ) with the calibration of previous molecular or fossil researches obtained from TimeTree ( http://www.timetree.org/ , Table S6 ). In this phylogenetic tree, the divergence time between Asian arowana and the common ancestor of African arowana and pirarucu was ∼106.1 million years ago (MYA), which was moderate to previous researches ( Cioffi et al., 2019 ; Du et al., 2019 ; Vialle et al., 2018 ). And the divergence time estimated here was close to the final separation time of South American and African continents in Afro-South American drift of Gondwana supercontinent happened at ∼110 MYA ( Rogers and Santosh, 2004 ).…”

“…And the divergence time estimated here was close to the final separation time of South American and African continents in Afro-South American drift of Gondwana supercontinent happened at ∼110 MYA ( Rogers and Santosh, 2004 ). Considering the previous evidences supporting that (1) Osteoglossinae fishes speciated along with the separation of South America, Antarctic, Australia, and Southeast Asia from ∼50.3MYA ( Cioffi et al., 2019 ); (2) Presently, Asian arowana only lives in Southeast Asia ( Mu et al., 2012 ); and (3) Africa has been identified as the taxonomic diversity center of Osteoglossiformes ( Wilson and Murray, 2008 ), we proposed that the ancestor of Asian arowana had migrated from Africa to Southeast Asia before or during the tectonic-mediated Gondwanan fragmentation (especially the fragmentation of Africa-South America, South America-Antarctica-Australia and the fragmentation of Southeast Asia-Australia) ( Figure 1 C). Then, the divergence time between African arowana and pirarucu was estimated as ∼59.2 MYA ( Figure 1 B), which was also close to the split time of North American and Eurasian continents (∼65 MYA or later) ( Rafferty, 2010 ; Rogers and Santosh, 2004 ).…”

“…Osteoglossidae contains two clades of Osteoglossinae and Heterotidinae , with species distributing in Asia, America, Africa, and Australia ( Wilson and Murray, 2008 ). The existence of Osteoglossiformes can be dated back to the Jurassic period according to fossil evidences ( Lavoue and Sullivan, 2004 ; Wilson and Murray, 2008 ), thus current species in Osteoglossiformes should had witnessed the break-up of the Gondwana supercontinent ( Cioffi et al., 2019 ; Kumazawa and Nishida, 2000 ; Lavoue, 2016 ). Therefore, Osteoglossiformes species, serving as models for biogeography, have been extensively studied in morphological and molecular evolution ( Hilton, 2001 , 2003 ; Kumazawa and Nishida, 2000 ; Lavoue and Sullivan, 2004 ; TANG et al., 2004 ), and also provide evidences for paleogeology.…”

Three genomes of Osteoglossidae shed light on ancient teleost evolution

“…1b ). Firstly, we calculated the divergence time of S. formosus and the common ancestor of H. niloticus and A. gigas at ∼106.1 Mya (± 20 Mya) [3, 8, 23], which is coincided with the separated time of South America and Africa continents by Afro-South American drift at ∼110 Mya[5]. At the original of separated time, the ancestor of S. formosus might live in South America.…”

“…The Osteoglossiformes fossils had been found earliest in the late Jurassic[2]. Therefore, it had witnessed the break-up of Gondwana supercontinent[3-5]. The evolutionary history of Osteoglossiformes species can represent a typical example of biogeography and have been studied extensively through morphological and molecular biological tools[2, 4, 6].…”