Nuclear and Mitochondrial Phylogenomics of the Sifakas Reveal Cryptic Variation in the Diademed Sifaka.

Melissa T R Hawkins, Carolyn A Bailey, Allyshia M Brown, Jen Tinsman, Ryan A Hagenson, Ryan R Culligan, Adena G Barela, Jean C Randriamanana, Jean F Ranaivoarisoa, John R Zaonarivelo, Edward E Louis
Author Information
  1. Melissa T R Hawkins: Department of Vertebrate Zoology, Division of Mammals, National Museum of Natural History, 10th and Constitution Ave, NW, Washington, DC 20560, USA. ORCID
  2. Carolyn A Bailey: Department of Conservation Genetics, Omaha's Henry Doorly Zoo & Aquarium, 3701 S 10th St, Omaha, NE 68107, USA.
  3. Allyshia M Brown: Department of Conservation Genetics, Omaha's Henry Doorly Zoo & Aquarium, 3701 S 10th St, Omaha, NE 68107, USA. ORCID
  4. Jen Tinsman: Department of Conservation Genetics, Omaha's Henry Doorly Zoo & Aquarium, 3701 S 10th St, Omaha, NE 68107, USA. ORCID
  5. Ryan A Hagenson: Department of Conservation Genetics, Omaha's Henry Doorly Zoo & Aquarium, 3701 S 10th St, Omaha, NE 68107, USA. ORCID
  6. Ryan R Culligan: Department of Conservation Genetics, Omaha's Henry Doorly Zoo & Aquarium, 3701 S 10th St, Omaha, NE 68107, USA. ORCID
  7. Adena G Barela: Department of Conservation Genetics, Omaha's Henry Doorly Zoo & Aquarium, 3701 S 10th St, Omaha, NE 68107, USA.
  8. Jean C Randriamanana: Madagascar Biodiversity Partnership, VO12 Bis a Manakambahiny, Antananarivo 101, Madagascar.
  9. Jean F Ranaivoarisoa: Anthropobiologie et Développement Durable, Faculty of Sciences, University of Antananarivo, Antananarivo 101, Madagascar. ORCID
  10. John R Zaonarivelo: Faculty of Sciences, Président du Collège des Enseignants, University of Antsiranana, Antsiranana 201, Madagascar.
  11. Edward E Louis: Department of Conservation Genetics, Omaha's Henry Doorly Zoo & Aquarium, 3701 S 10th St, Omaha, NE 68107, USA.

Abstract

The most comprehensive phylogenomic reconstruction to date was generated on all nominal taxa within the lemur genus Propithecus. Over 200 wild-caught individuals were included in this study to evaluate the intra and interspecific relationships across this genus. Ultraconserved Elements (UCEs) resulted in well-supported phylogenomic trees. Complete mitochondrial genomes (CMGs) largely agreed with the UCEs, except where a mitochondrial introgression was detected between one clade of the diademed sifaka (Propithecus diadema) and the Milne-Edwards sifaka (P. edwardsi). Additionally, the crowned (P. coronatus) and Von der Decken’s (P. deckeni) sifakas belonged to a single admixed lineage from UCEs. Further sampling across these two species is warranted to determine if our sampling represents a hybrid zone. P. diadema recovered two well-supported clades, which were dated and estimated as being ancient as the split between the Perrier’s (P. perrierii) and silky (P. candidus) sifakas. The reconstructed demographic history of the two clades also varied over time. We then modeled the modern ecological niches of the two cryptic P. diadema clades and found that they were significantly diverged (p < 0.01). These ecological differences result in a very limited zone of geographic overlap for the P. diadema clades (<60 km2). Niche models also revealed that the Onive River acts as a potential barrier to dispersal between P. diadema and P. edwardsi. Further taxonomic work is required on P. diadema to determine if its taxonomic status should be revised. This first genomic evaluation of the genus resolved the relationships between the taxa and the recovered cryptic diversity within one species.

Keywords

References

  1. Biol Lett. 2008 Oct 23;4(5):590-4 [PMID: 18664414]
  2. Syst Biol. 2021 Feb 10;70(2):203-218 [PMID: 32642760]
  3. Mol Phylogenet Evol. 2010 Jun;55(3):833-45 [PMID: 20211744]
  4. Mol Biol Evol. 2013 Apr;30(4):772-80 [PMID: 23329690]
  5. BMC Evol Biol. 2014 Mar 24;14(1):57 [PMID: 24661555]
  6. Am J Phys Anthropol. 2004 Sep;125(1):61-72 [PMID: 15293332]
  7. Biol Lett. 2012 Oct 23;8(5):783-6 [PMID: 22593086]
  8. BMC Evol Biol. 2020 Aug 8;20(1):97 [PMID: 32770933]
  9. Philos Trans R Soc Lond B Biol Sci. 2014 Feb 17;369(1639):20130089 [PMID: 24535397]
  10. Syst Biol. 2016 Sep;65(5):772-91 [PMID: 27113475]
  11. Syst Biol. 2011 Oct;60(5):661-7 [PMID: 21447481]
  12. Science. 2006 May 19;312(5776):1063-5 [PMID: 16709785]
  13. Genome Res. 2012 Apr;22(4):746-54 [PMID: 22207614]
  14. RNA Biol. 2008 Jul-Sep;5(3):132-4 [PMID: 18708752]
  15. Am J Primatol. 2005 Nov;67(3):347-64 [PMID: 16287105]
  16. Am J Primatol. 2001 Jan;53(1):1-17 [PMID: 11195201]
  17. J Mammal. 2016 Jun 9;97(3):663-688 [PMID: 29692469]
  18. Front Zool. 2013 Nov 14;10(1):70 [PMID: 24228694]
  19. Physiol Behav. 1999 Jul;66(5):855-61 [PMID: 10405114]
  20. Mol Biol Evol. 2018 Jul 1;35(7):1798-1811 [PMID: 29659989]
  21. Bioinformatics. 2014 Aug 1;30(15):2114-20 [PMID: 24695404]
  22. Bioinformatics. 2014 May 1;30(9):1312-3 [PMID: 24451623]
  23. Mol Ecol. 2020 Nov;29(21):4074-4090 [PMID: 32911576]
  24. Heredity (Edinb). 2020 Jan;124(1):236-251 [PMID: 31435007]
  25. Genome Res. 2012 May;22(5):939-46 [PMID: 22267522]
  26. J Hum Evol. 2000 Oct;39(4):381-91 [PMID: 11006047]
  27. Mol Biol Evol. 2012 Aug;29(8):1969-73 [PMID: 22367748]
  28. Folia Primatol (Basel). 1998;69(2):106-14 [PMID: 9583951]
  29. PLoS Comput Biol. 2014 Apr 10;10(4):e1003537 [PMID: 24722319]
  30. Evolution. 2008 Nov;62(11):2868-83 [PMID: 18752605]
  31. Philos Trans A Math Phys Eng Sci. 2005 Jan 15;363(1826):55-9 [PMID: 15598621]
  32. BMC Evol Biol. 2007 Nov 08;7:214 [PMID: 17996036]
  33. Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11325-30 [PMID: 11005834]
  34. J Hum Evol. 2015 Feb;79:45-54 [PMID: 25523037]
  35. Evolution. 2009 Apr;63(4):959-67 [PMID: 19210532]
  36. Nucleic Acids Res. 2016 Jul 8;44(W1):W232-5 [PMID: 27084950]
  37. Mol Phylogenet Evol. 2017 Feb;107:282-292 [PMID: 27789326]
  38. Nucleic Acids Res. 2013 Jul;41(Web Server issue):W238-41 [PMID: 23661681]
  39. J Hered. 2017 Mar 1;108(2):107-119 [PMID: 28173059]
  40. J Hum Evol. 2005 Mar;48(3):259-77 [PMID: 15737393]
  41. Syst Biol. 2012 Oct;61(5):717-26 [PMID: 22232343]
  42. Bioinformatics. 2003 Aug 12;19(12):1572-4 [PMID: 12912839]
  43. Mol Biol Evol. 2015 Jan;32(1):268-74 [PMID: 25371430]
  44. BMC Evol Biol. 2016 Apr 14;16:80 [PMID: 27075887]
  45. Sci Adv. 2021 Apr 23;7(17): [PMID: 33893095]
  46. Bioinformatics. 2016 Mar 1;32(5):786-8 [PMID: 26530724]
  47. Mol Biol Evol. 2012 Jun;29(6):1695-701 [PMID: 22319168]
  48. Mol Ecol. 2017 Oct;26(19):5203-5222 [PMID: 28488335]
  49. Ecol Evol. 2015 Mar;5(6):1131-42 [PMID: 25859320]
  50. Chromosome Res. 2011 Feb;19(2):209-24 [PMID: 21336668]

MeSH Term

Animals
Ecosystem
Humans
Indriidae
Mitochondria
Phylogeny
Sea Urchins

Word Cloud

Created with Highcharts 10.0.0PdiadematwocladesgenusPropithecusUCEsecologicalphylogenomictaxawithinrelationshipsacrossUltraconservedElementswell-supportedmitochondrialonesifakaedwardsisifakassamplingspeciesdeterminezonerecoveredalsocryptictaxonomiccomprehensivereconstructiondategeneratednominallemur200wild-caughtindividualsincludedstudyevaluateintrainterspecificresultedtreesCompletegenomesCMGslargelyagreedexceptintrogressiondetectedcladediademedMilne-EdwardsAdditionallycrownedcoronatusVonderDecken’sdeckenibelongedsingleadmixedlineagewarrantedrepresentshybriddatedestimatedancientsplitPerrier’sperrieriisilkycandidusreconstructeddemographichistoryvariedtimemodeledmodernnichesfoundsignificantlydivergedp<001differencesresultlimitedgeographicoverlap<60km2NichemodelsrevealedOniveRiveractspotentialbarrierdispersalworkrequiredstatusrevisedfirstgenomicevaluationresolveddiversityNuclearMitochondrialPhylogenomicsSifakasRevealCrypticVariationDiademedSifakaIndriidaeMadagascarnichemodelinggenomics

Similar Articles

Cited By