Ancestral chromosomal signatures of Paenungulata (Afroteria) reveal the karyotype of Amazonian manatee (Trichechus inunguis, Sirenia: Trichechidae) as the oldest among American manatees
Abstract Background Chromosomal painting in manatees has clarified questions about the rapid evolution of sirenians within the Paenungulata clade. Further cytogenetic studies in Afrotherian species may provide information about their evolutionary dynamics, revealing important insights into the ances...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2023-01-01
|
| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12864-023-09129-3 |
| _version_ | 1811175974170001408 |
|---|---|
| author | Flávia dos Santos Tavares Willam Oliveira da Silva Malcolm Andrew Ferguson-Smith Alex Garcia Cavalleiro de Macedo Klautau Jairo Moura Oliveira Angélica Lúcia Figueiredo Rodrigues Gabriel Melo-Santos Julio Cesar Pieczarka Cleusa Yoshiko Nagamachi Renata Coelho Rodrigues Noronha |
| author_facet | Flávia dos Santos Tavares Willam Oliveira da Silva Malcolm Andrew Ferguson-Smith Alex Garcia Cavalleiro de Macedo Klautau Jairo Moura Oliveira Angélica Lúcia Figueiredo Rodrigues Gabriel Melo-Santos Julio Cesar Pieczarka Cleusa Yoshiko Nagamachi Renata Coelho Rodrigues Noronha |
| author_sort | Flávia dos Santos Tavares |
| collection | DOAJ |
| description | Abstract Background Chromosomal painting in manatees has clarified questions about the rapid evolution of sirenians within the Paenungulata clade. Further cytogenetic studies in Afrotherian species may provide information about their evolutionary dynamics, revealing important insights into the ancestral karyotype in the clade representatives. The karyotype of Trichechus inunguis (TIN, Amazonian manatee) was investigated by chromosome painting, using probes from Trichechus manatus latirostris (TML, Florida manatee) to analyze the homeologies between these sirenians. Results A high similarity was found between these species, with 31 homologous segments in TIN, nineteen of which are whole autosomes, besides the X and Y sex chromosomes. Four chromosomes from TML (4, 6, 8, and 9) resulted in two hybridization signals, totaling eight acrocentrics in the TIN karyotype. This study confirmed in TIN the chromosomal associations of Homo sapiens (HSA) shared in Afrotheria, such as the 5/21 synteny, and in the Paenungulata clade with the syntenies HSA 2/3, 8/22, and 18/19, in addition to the absence of HSA 4/8 common in eutherian ancestral karyotype (EAK). Conclusions TIN shares more conserved chromosomal signals with the Paenungulata Ancestral Karyotype (APK, 2n = 58) than Procavia capensis (Hyracoidea), Loxodonta africana (Proboscidea) and TML (Sirenia), where TML presents less conserved signals with APK, demonstrating that its karyotype is the most derived among the representatives of Paenungulata. The chromosomal changes that evolved from APK to the T. manatus and T. inunguis karyotypes (7 and 4 changes, respectively) are more substantial within the Trichechus genus compared to other paenungulates. Among these species, T. inunguis presents conserved traits of APK in the American manatee genus. Consequently, the karyotype of T. manatus is more derived than that of T. inunguis. |
| first_indexed | 2024-04-10T19:45:37Z |
| format | Article |
| id | doaj.art-bfe92ccc26094a82a019efb6c0848e17 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-04-10T19:45:37Z |
| publishDate | 2023-01-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-bfe92ccc26094a82a019efb6c0848e172023-01-29T12:05:12ZengBMCBMC Genomics1471-21642023-01-0124111010.1186/s12864-023-09129-3Ancestral chromosomal signatures of Paenungulata (Afroteria) reveal the karyotype of Amazonian manatee (Trichechus inunguis, Sirenia: Trichechidae) as the oldest among American manateesFlávia dos Santos Tavares0Willam Oliveira da Silva1Malcolm Andrew Ferguson-Smith2Alex Garcia Cavalleiro de Macedo Klautau3Jairo Moura Oliveira4Angélica Lúcia Figueiredo Rodrigues5Gabriel Melo-Santos6Julio Cesar Pieczarka7Cleusa Yoshiko Nagamachi8Renata Coelho Rodrigues Noronha9Laboratório de Citogenética, Centro de Estudos Avançados da Biodiversidade, Instituto de Ciências Biológicas, Universidade Federal Do Pará (UFPA)Laboratório de Citogenética, Centro de Estudos Avançados da Biodiversidade, Instituto de Ciências Biológicas, Universidade Federal Do Pará (UFPA)Cambridge Resource Centre for Comparative Genomics, Department of Veterinary Medicine, University of CambridgeCentro Nacional de Pesquisa e Conservação de Mamíferos Aquáticos, Instituto Chico Mendes de Conservação da BiodiversidadeZoological Park of Santarém – Universidade da Amazônia (ZOOUNAMA)Instituto de Biologia e Conservação de Mamíferos Aquáticos da Amazônia, Universidade Federal Rural da Amazônia (UFRA)Instituto de Biologia e Conservação de Mamíferos Aquáticos da Amazônia, Universidade Federal Rural da Amazônia (UFRA)Laboratório de Citogenética, Centro de Estudos Avançados da Biodiversidade, Instituto de Ciências Biológicas, Universidade Federal Do Pará (UFPA)Laboratório de Citogenética, Centro de Estudos Avançados da Biodiversidade, Instituto de Ciências Biológicas, Universidade Federal Do Pará (UFPA)Laboratório de Citogenética, Centro de Estudos Avançados da Biodiversidade, Instituto de Ciências Biológicas, Universidade Federal Do Pará (UFPA)Abstract Background Chromosomal painting in manatees has clarified questions about the rapid evolution of sirenians within the Paenungulata clade. Further cytogenetic studies in Afrotherian species may provide information about their evolutionary dynamics, revealing important insights into the ancestral karyotype in the clade representatives. The karyotype of Trichechus inunguis (TIN, Amazonian manatee) was investigated by chromosome painting, using probes from Trichechus manatus latirostris (TML, Florida manatee) to analyze the homeologies between these sirenians. Results A high similarity was found between these species, with 31 homologous segments in TIN, nineteen of which are whole autosomes, besides the X and Y sex chromosomes. Four chromosomes from TML (4, 6, 8, and 9) resulted in two hybridization signals, totaling eight acrocentrics in the TIN karyotype. This study confirmed in TIN the chromosomal associations of Homo sapiens (HSA) shared in Afrotheria, such as the 5/21 synteny, and in the Paenungulata clade with the syntenies HSA 2/3, 8/22, and 18/19, in addition to the absence of HSA 4/8 common in eutherian ancestral karyotype (EAK). Conclusions TIN shares more conserved chromosomal signals with the Paenungulata Ancestral Karyotype (APK, 2n = 58) than Procavia capensis (Hyracoidea), Loxodonta africana (Proboscidea) and TML (Sirenia), where TML presents less conserved signals with APK, demonstrating that its karyotype is the most derived among the representatives of Paenungulata. The chromosomal changes that evolved from APK to the T. manatus and T. inunguis karyotypes (7 and 4 changes, respectively) are more substantial within the Trichechus genus compared to other paenungulates. Among these species, T. inunguis presents conserved traits of APK in the American manatee genus. Consequently, the karyotype of T. manatus is more derived than that of T. inunguis.https://doi.org/10.1186/s12864-023-09129-3Chromosomal evolutionSireniansAncestral karyotypeZOO-FISH |
| spellingShingle | Flávia dos Santos Tavares Willam Oliveira da Silva Malcolm Andrew Ferguson-Smith Alex Garcia Cavalleiro de Macedo Klautau Jairo Moura Oliveira Angélica Lúcia Figueiredo Rodrigues Gabriel Melo-Santos Julio Cesar Pieczarka Cleusa Yoshiko Nagamachi Renata Coelho Rodrigues Noronha Ancestral chromosomal signatures of Paenungulata (Afroteria) reveal the karyotype of Amazonian manatee (Trichechus inunguis, Sirenia: Trichechidae) as the oldest among American manatees BMC Genomics Chromosomal evolution Sirenians Ancestral karyotype ZOO-FISH |
| title | Ancestral chromosomal signatures of Paenungulata (Afroteria) reveal the karyotype of Amazonian manatee (Trichechus inunguis, Sirenia: Trichechidae) as the oldest among American manatees |
| title_full | Ancestral chromosomal signatures of Paenungulata (Afroteria) reveal the karyotype of Amazonian manatee (Trichechus inunguis, Sirenia: Trichechidae) as the oldest among American manatees |
| title_fullStr | Ancestral chromosomal signatures of Paenungulata (Afroteria) reveal the karyotype of Amazonian manatee (Trichechus inunguis, Sirenia: Trichechidae) as the oldest among American manatees |
| title_full_unstemmed | Ancestral chromosomal signatures of Paenungulata (Afroteria) reveal the karyotype of Amazonian manatee (Trichechus inunguis, Sirenia: Trichechidae) as the oldest among American manatees |
| title_short | Ancestral chromosomal signatures of Paenungulata (Afroteria) reveal the karyotype of Amazonian manatee (Trichechus inunguis, Sirenia: Trichechidae) as the oldest among American manatees |
| title_sort | ancestral chromosomal signatures of paenungulata afroteria reveal the karyotype of amazonian manatee trichechus inunguis sirenia trichechidae as the oldest among american manatees |
| topic | Chromosomal evolution Sirenians Ancestral karyotype ZOO-FISH |
| url | https://doi.org/10.1186/s12864-023-09129-3 |
| work_keys_str_mv | AT flaviadossantostavares ancestralchromosomalsignaturesofpaenungulataafroteriarevealthekaryotypeofamazonianmanateetrichechusinunguissireniatrichechidaeastheoldestamongamericanmanatees AT willamoliveiradasilva ancestralchromosomalsignaturesofpaenungulataafroteriarevealthekaryotypeofamazonianmanateetrichechusinunguissireniatrichechidaeastheoldestamongamericanmanatees AT malcolmandrewfergusonsmith ancestralchromosomalsignaturesofpaenungulataafroteriarevealthekaryotypeofamazonianmanateetrichechusinunguissireniatrichechidaeastheoldestamongamericanmanatees AT alexgarciacavalleirodemacedoklautau ancestralchromosomalsignaturesofpaenungulataafroteriarevealthekaryotypeofamazonianmanateetrichechusinunguissireniatrichechidaeastheoldestamongamericanmanatees AT jairomouraoliveira ancestralchromosomalsignaturesofpaenungulataafroteriarevealthekaryotypeofamazonianmanateetrichechusinunguissireniatrichechidaeastheoldestamongamericanmanatees AT angelicaluciafigueiredorodrigues ancestralchromosomalsignaturesofpaenungulataafroteriarevealthekaryotypeofamazonianmanateetrichechusinunguissireniatrichechidaeastheoldestamongamericanmanatees AT gabrielmelosantos ancestralchromosomalsignaturesofpaenungulataafroteriarevealthekaryotypeofamazonianmanateetrichechusinunguissireniatrichechidaeastheoldestamongamericanmanatees AT juliocesarpieczarka ancestralchromosomalsignaturesofpaenungulataafroteriarevealthekaryotypeofamazonianmanateetrichechusinunguissireniatrichechidaeastheoldestamongamericanmanatees AT cleusayoshikonagamachi ancestralchromosomalsignaturesofpaenungulataafroteriarevealthekaryotypeofamazonianmanateetrichechusinunguissireniatrichechidaeastheoldestamongamericanmanatees AT renatacoelhorodriguesnoronha ancestralchromosomalsignaturesofpaenungulataafroteriarevealthekaryotypeofamazonianmanateetrichechusinunguissireniatrichechidaeastheoldestamongamericanmanatees |