Early shape divergence of developmental trajectories in the jaw of galeomorph sharks.

Faviel A López-Romero, Fidji Berio, Daniel Abed-Navandi, Jürgen Kriwet
Author Information
  1. Faviel A López-Romero: Department of Palaeontology, University of Vienna, Althanstraße 14, Geocenter, 1090, Vienna, Austria. faviel.l.r@gmail.com. ORCID
  2. Fidji Berio: ISEM, CNRS, IRD, EPHE, Univ. Montpellier, Montpellier, France.
  3. Daniel Abed-Navandi: Haus des Meeres - Aqua Terra Zoo, Fritz Gruenbaumpl. 1, 1060, Wien, Austria.
  4. Jürgen Kriwet: Department of Palaeontology, University of Vienna, Althanstraße 14, Geocenter, 1090, Vienna, Austria.

Abstract

BACKGROUND: The onset of morphological differences between related groups can be tracked at early stages during embryological development. This is expressed in functional traits that start with minor variations, but eventually diverge to defined specific morphologies. Several processes during this period, like proliferation, remodelling, and apoptosis for instance, can account for the variability observed between related groups. Morphological divergence through development is often associated with the hourglass model, in which early stages display higher variability and reach a conserved point with reduced variability from which divergence occurs again to the final phenotype.
RESULTS: Here we explored the patterns of developmental shape changes in the lower jaw of two shark species, the bamboo shark (Chiloscyllium punctatum) and the catshark (Scyliorhinus canicula). These two species present marked differences in their foraging behaviour, which is reflected in their adult jaw morphology. By tracing the developmental sequence of the cartilage condensation, we identified the onset of cartilage for both species at around stage 31. Other structures that developed later without a noticeable anlage were the labial cartilages, which appear at around stage 33. We observed that the lower jaw displays striking differences in shape from the earliest moments, without any overlap in shape through the compared stages.
CONCLUSIONS: The differences observed are also reflected in the functional variation in feeding mechanism between both species. Likewise, the trajectory analysis shows that the main differences are in the magnitude of the shape change through time. Both species follow a unique trajectory, which is explained by the timing between stages.

Keywords

References

  1. Development. 2014 Mar;141(5):1059-63 [PMID: 24550113]
  2. Dev Biol. 2011 Aug 1;356(1):28-39 [PMID: 21600197]
  3. Mitochondrial DNA A DNA Mapp Seq Anal. 2018 Aug;29(6):867-878 [PMID: 28927318]
  4. CSH Protoc. 2008 Dec 01;2008:pdb.emo111 [PMID: 21356737]
  5. Development. 2008 Dec;135(23):3947-58 [PMID: 18987028]
  6. J Appl Ichthyol. 2012 Jun 1;28(3):341-345 [PMID: 26566297]
  7. Trends Genet. 2013 Dec;29(12):712-22 [PMID: 24120296]
  8. Nature. 2010 Dec 9;468(7325):815-8 [PMID: 21150997]
  9. Proc Biol Sci. 2017 Aug 16;284(1860): [PMID: 28768892]
  10. Evodevo. 2014 Nov 03;5(1):40 [PMID: 25419450]
  11. Evolution. 2015 Jul;69(7):1665-77 [PMID: 25964090]
  12. J Exp Biol. 1997;200(Pt 8):1255-69 [PMID: 9319118]
  13. J Fish Biol. 2019 Feb;94(2):313-319 [PMID: 30565231]
  14. J Exp Biol. 2008 Oct;211(Pt 19):3128-38 [PMID: 18805812]
  15. Nat Commun. 2014 Apr 03;5:3629 [PMID: 24699776]
  16. Proc Natl Acad Sci U S A. 2009 Apr 7;106(14):5720-4 [PMID: 19321424]
  17. Dev Dyn. 2015 Sep;244(9):1158-1167 [PMID: 25703037]
  18. Development. 2014 Feb;141(3):674-84 [PMID: 24449843]
  19. Zoology (Jena). 2009;112(5):351-61 [PMID: 19428230]
  20. Integr Comp Biol. 2016 Sep;56(3):442-8 [PMID: 27371386]
  21. BMC Ecol Evol. 2021 Oct 21;21(1):192 [PMID: 34674635]
  22. J Morphol. 1994 Nov;222(2):175-190 [PMID: 29865406]
  23. Anat Rec (Hoboken). 2008 Sep;291(9):1079-87 [PMID: 18493933]
  24. Dev Dyn. 2015 Sep;244(9):1168-1178 [PMID: 26150089]
  25. J Fish Biol. 2020 Jul;97(1):257-264 [PMID: 32383486]
  26. J Morphol. 1998 Apr;236(1):25-47 [PMID: 29852708]
  27. J Morphol. 2004 Apr;260(1):1-12 [PMID: 15052592]
  28. Biotech Histochem. 2007 Feb;82(1):23-8 [PMID: 17510811]
  29. Zoolog Sci. 2008 Oct;25(10):990-8 [PMID: 19267635]
  30. Biol Rev Camb Philos Soc. 2016 Aug;91(3):611-57 [PMID: 25899041]
  31. J Morphol. 1999 Jan;239(1):45-59 [PMID: 29847876]
  32. Front Cell Dev Biol. 2020 Aug 28;8:821 [PMID: 32984323]
  33. J Morphol. 2009 May;270(5):628-43 [PMID: 19117064]
  34. Zoology (Jena). 2010 Aug;113(4):199-212 [PMID: 20817493]
  35. Evol Dev. 2012 Jan-Feb;14(1):76-92 [PMID: 23016976]
  36. Nat Ecol Evol. 2018 Nov;2(11):1761-1771 [PMID: 30297745]
  37. J Anat. 2021 May;238(5):1082-1105 [PMID: 33415764]
  38. Proc Biol Sci. 2014 Oct 22;281(1793): [PMID: 25209942]
  39. Proc Natl Acad Sci U S A. 2015 Dec 29;112(52):15940-5 [PMID: 26644578]
  40. J Exp Biol. 2019 Mar 1;222(Pt 5): [PMID: 30824570]
  41. Elife. 2021 Feb 09;10: [PMID: 33560225]
  42. Evodevo. 2015 Jun 28;6:25 [PMID: 26225206]
  43. J Hum Evol. 2004 Jun;46(6):679-97 [PMID: 15183670]
  44. Integr Comp Biol. 2016 Sep;56(3):404-15 [PMID: 27260858]
  45. Dev Dyn. 2018 May;247(5):712-723 [PMID: 29396887]
  46. Integr Comp Biol. 2007 Jul;47(1):55-69 [PMID: 21672820]
  47. Development. 2015 Feb 1;142(3):567-74 [PMID: 25605783]
  48. Curr Top Dev Biol. 2015;115:299-320 [PMID: 26589930]
  49. J Fish Biol. 2020 Jul;97(1):212-224 [PMID: 32307702]
  50. J Fish Biol. 2016 Mar;88(3):837-1037 [PMID: 26860638]
  51. Nat Commun. 2015 Apr 14;6:6698 [PMID: 25868783]
  52. Evodevo. 2014 Feb 05;5(1):8 [PMID: 24499543]
  53. Dev Cell. 2012 May 15;22(5):903-4 [PMID: 22595663]
  54. J Exp Zool B Mol Dev Evol. 2010 Mar 15;314(2):166-78 [PMID: 19757482]
  55. Theory Biosci. 2005 Nov;124(2):145-63 [PMID: 17046353]
  56. Development. 2014 Dec;141(24):4649-55 [PMID: 25468934]
  57. Mol Phylogenet Evol. 2006 May;39(2):384-91 [PMID: 16293425]
  58. J Morphol. 2007 Aug;268(8):664-82 [PMID: 17458888]

Grants

  1. P 33820/Austrian Science Fund FWF
  2. P33820/Austrian Science Fund

Word Cloud

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