The ultimate database to (re)set the evolutionary history of primate genital bones.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
27 05 2021
27 05 2021
Historique:
received:
16
02
2021
accepted:
17
05
2021
entrez:
28
5
2021
pubmed:
29
5
2021
medline:
9
11
2021
Statut:
epublish
Résumé
Scientific literature concerning genital bones in primates consists of both ancient works (dating back to the nineteenth century) and more recent revisions/meta-analyses, which, however, are not always so detailed or exhaustive. Based on a thorough analysis, several conflicting data, inaccurate references, and questionable claims have emerged. We generated a binary matrix of genital bone occurrence data, considering only data at the species level, based on (1) a rigorous literature search protocol, (2) raw data (collected exclusively from primary literature), (3) an updated taxonomy (often tracing back to the species taxonomic history) and (4) new occurrence data from scanned genitals of fresh and museum specimens (using micro-computed tomography-micro-CT). Thanks to this methodological approach, we almost doubled available occurrence data so far, avoiding any arbitrary extension of generic data to conspecific species. This practice, in fact, has been recently responsible for an overestimation of the occurrence data, definitively flattening the interspecific variability. We performed the ancestral state reconstruction analysis of genital bone occurrence and results were mapped onto the most updated phylogeny of primates. As for baculum, we definitively demonstrated its simplesiomorphy for the entire order. As for baubellum, we interpreted all scattered absences as losses, actually proposing (for the first time) a simplesiomorphic state for the clitoral bone as well. The occurrence data obtained, while indirectly confirming the baculum/baubellum homology (i.e., for each baubellum a baculum was invariably present), could also directly demonstrate an intra-specific variability affecting ossa genitalia occurrence. With our results, we established a radically improved and updated database about the occurrence of genital bones in primates, available for further comparative analyses.
Identifiants
pubmed: 34045627
doi: 10.1038/s41598-021-90787-2
pii: 10.1038/s41598-021-90787-2
pmc: PMC8160331
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
11245Références
Brocke, vom J.et al. Reconstructing the giant: On the importance of rigour in documenting the literature search process. In ECIS 2009 Proceedings 161 (2009).
Newton, I. & Hooke, R. Isaac Newton letter to Robert Hooke (1675).
Weatherall, D. J. On the shoulders of giants. The Lancet 381(9861), 105–106 (2013).
doi: 10.1016/S0140-6736(13)60034-3
vom Brocke, J. et al. Standing on the shoulders of giants: Challenges and recommendations of literature search in information systems research. CAIS 37(9), 205–224 (2015).
Grandidier, A. Observations sur les Propitheques de Madagascar. C. R. Acad. Sci. 72, 231–232 (1871).
Harcourt, A. H. & Gardiner, J. Sexual selection and genital anatomy of male primates. Proc. R. Soc. B 255(1342), 47–53 (1994).
pubmed: 8153136
doi: 10.1098/rspb.1994.0007
Gerhardt, U. Ueber das Vorkommen eines Penis-und Clitorisknochens bei Hylobatiden. Ann. Anat. 35, 353–358 (1909).
von Pehrson, T. Beitrage zur Kenntnis des Os penis der Prosimier. Ann. Anat. 37, 225–231 (1910).
von Pehrson, T. Zur Morphologie der männlichen Kopulationsorgane der Säugetiere; insbesondere der Versuch einer vergleichend-anatomischen Studie über den Penis der Primaten, einschließlich des Menschen. Brain Struct. Funct. 86, 71–119 (1928).
von Pehrson, T. Beiträge zur Kenntnis der äusseren weiblichen Genitalien bei Affen, Halbaffen, und Insectivoren. Ann. Anat. 46, 161–179 (1914).
Pocock, R. I. On the external characters of the Lemurs and of Tarsius. J Zool. 88, 19–53 (1918).
Pocock, R. I. On the external characters of the South American Monkeys. J Zool. 90, 91–113 (1920).
Pocock, R. I. The external characters of the Catarrhine Monkeys and Apes. J Zool. 95, 1479–1579 (1925).
Wislocki, G. B. The external genitalia of the simian primates. Hum. Biol. 8, 309–347 (1936).
Hill, O. W. C. Primates-Comparative Anatomy and Taxonomy (University Press, 1953–1974).
Harms, J. W. Volume I: Systematik. Phylogenie. Ontogenie. In Primatologia. Handbuch der Primatenkunde (eds Hofer, H. et al.) (Karger Publishers, 1956).
Ioannou, J. M. Vol. 6: Female reproductive organs. In Comparative Reproduction of Nonhuman Primates (ed. Hafex, E. S. E.) 131–159 (Thomas C. C. Publisher, 1971).
Hershkovitz, P. Vol. 1(2): 14. External genitalia and accessory structures. In Living New World Monkeys (Platyrrhini) with an Introduction to Primates (ed. Hershkovitz, P.) 112–119 (The University Chicago Press, 1977).
Hershkovitz, P. Male external genitalia of non-prehensile tailed South-American monkeys. Part I. Subfamily Pitheciinae, Family Cebidae. Fieldiana Zool. 73, 1–17 (1993).
Dixson, A. F. Baculum length and copulatory behavior in primates. Am. J. Primatol. 13, 51–60 (1987).
pubmed: 31973483
doi: 10.1002/ajp.1350130107
Geissmann, T. & Lim, K. K. P. Extraction of bacula of tanned gibbons skins. Raffles Bull. Zool. 42(4), 775–780 (1994).
Anderson, M. J. Penile morphology and classification of bush babies (subfamily Galagoninae). Int. J. Primatol. 21(5), 815–836 (2000).
doi: 10.1023/A:1005542609002
Carosi, M., Ulland, A. E., Gerald, M. S. & Suomi, S. J. Male-like external genitalia in female tufted capuchins (Cebus apella), and the presence of a clitoral bone (baubellum): A cross-sectional study. Folia Primatol. 72, 149 (2001).
Dixson, A. F., Pissinatti, A. & Anderson, M. J. Observations on genital morphology and anatomy of a hybrid male muriqui (genus Brachyteles). Folia Primatol. 75(2), 61–69 (2004).
doi: 10.1159/000076264
Dixson, A. F. Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes, and Humans (Oxford University Press, 2012).
doi: 10.1093/acprof:osobl/9780199544646.001.0001
Schultz, N. G., Lough-Stevens, M., Abreu, E., Orr, T. & Dean, M. D. The Baculum was gained and lost multiple times during mammalian evolution. Integr. Comp. Biol. 56, 644–656 (2016).
pubmed: 27252214
pmcid: 6080509
doi: 10.1093/icb/icw034
Orr, T. J. & Brennan, P. L. All features great and small—The potential roles of the baculum and penile spines in mammals. Integr. Comp. Biol. 56(4), 635–643 (2016).
pubmed: 27371391
doi: 10.1093/icb/icw057
Brindle, M. & Opie, C. Postcopulatory sexual selection influences baculum evolution in primates and carnivores. Proc. R. Soc. B 283, 20161736. https://doi.org/10.1098/rspb.2016.1736 (2016).
doi: 10.1098/rspb.2016.1736
pubmed: 27974519
pmcid: 5204150
Lough-Stevens, M., Schultz, N. G. & Dean, M. D. The baubellum is more developmentally and evolutionarily labile than the baculum. Ecol. Evol. 8(2), 1073–1083 (2018).
pubmed: 29375780
doi: 10.1002/ece3.3634
Dixson, A. F. & Anderson, M. Sexual selection and the comparative anatomy of reproduction in monkeys, apes, and human beings. Annu. Rev. Sex Res. 12(1), 121–144 (2001).
pubmed: 12666739
Dixson, A. F. Observations on the evolution of the genitalia and copulatory behaviour in male primates. J. Zool. 213, 423–443 (1987).
doi: 10.1111/j.1469-7998.1987.tb03718.x
Dixson, A. F. Baculum length and copulatory behaviour in carnivores and pinnipeds (Grand Order Ferae). J. Zool. 235, 67–76 (1995).
doi: 10.1111/j.1469-7998.1995.tb05128.x
Miller, E. H., Jones, I. L. & Stenson, G. B. Baculum and testes of the hooded seal (Cystophora cristata): Growth and size-scaling and their relationships to sexual selection. Can. J. Zool. 77, 470–479 (1999).
doi: 10.1139/z98-233
Hosken, D., Jones, K., Chipperfield, K. & Dixson, A. Is the bat os penis sexually selected? Behav. Ecol. Sociobiol. 50, 450–460 (2001).
doi: 10.1007/s002650100389
Lariviére, S. & Ferguson, S. H. On the evolution of the mammalian baculum: Vaginal friction, prolonged intromission or induced ovulation? Mamm. Rev. 32, 283–294 (2002).
doi: 10.1046/j.1365-2907.2002.00112.x
Miller, E. H. & Burton, L. E. It’s all relative: Allometry and variation in the baculum (os penis) of the harp seal, Pagophilus groenlandicus (Carnivora: Phocidae). Biol. J. Linn. Soc. 72, 345–355 (2001).
doi: 10.1111/j.1095-8312.2001.tb01322.x
Lüpold, S., McElligott, A. G. & Hosken, D. J. Bat genitalia: Allometry, variation and good genes. Biol. J. Linn. Soc. 83, 497–507 (2004).
doi: 10.1111/j.1095-8312.2004.00407.x
Ramm, S. A. Sexual selection and genital evolution in mammals: A phylogenetic analysis of baculum length. Am. Nat. 169, 360–369 (2007).
pubmed: 17238128
doi: 10.1086/510688
Tasikas, D., Fairn, E., Laurence, S. & Schulte-Hostedde, A. Baculum variation and allometry in the muskrat (Ondatra zibethicus): A case for sexual selection. Evol. Ecol. 23(2), 223–232 (2009).
doi: 10.1007/s10682-007-9216-2
Ramm, S., Khoo, L. & Stockley, P. Sexual selection and the rodent baculum: An intraspecific study in the house mouse (Mus musculus domesticus). Genetica 138, 129–137 (2010).
pubmed: 19597945
doi: 10.1007/s10709-009-9385-8
Schulte-Hostedde, A. I., Bowman, J. & Middel, K. R. Allometry of the baculum and sexual size dimorphism in American martens and fishers (Mammalia: Mustelidae). Biol. J. Linn. Soc. 104, 955–963 (2011).
doi: 10.1111/j.1095-8312.2011.01775.x
Fitzpatrick, J. L., Almbro, M., Gonzalez-Voyer, A., Kolm, N. & Simmons, L. W. Male contest competition and the coevolution of weaponry and testes in pinnipeds. Evolution 66, 595–604 (2012).
doi: 10.1111/j.1558-5646.2012.01713.x
Simmons, L. W. & Firman, R. C. Experimental evidence for the evolution of the mammalian baculum by sexual selection. Evolution 68, 276–283 (2013).
pubmed: 24372607
doi: 10.1111/evo.12229
Stockley, P. et al. Baculum morphology predicts reproductive success of male house mice under sexual selection. BMC Biol. 11, 66. https://doi.org/10.1186/1741-7007-11-66 (2013).
doi: 10.1186/1741-7007-11-66
pubmed: 23800051
pmcid: 3693876
Simokawa, S. Einige Bemerkungen fiber den Clitorisknochen Keijo. J. Med. 9, 273–282 (1938).
Jellison, W. L. A suggested homolog of the os penis or baculum of mammals. J. Mammal. 26, 146–147 (1945).
doi: 10.2307/1375090
Layne, J. N. The os clitoridis of some North American Sciuridae. J. Mamm. 35, 357–366 (1954).
doi: 10.2307/1375960
Burt, W. H. A study of the baculum in the genera Perognathus and Dipodomys. J. Mammal. 17, 145–156 (1936).
doi: 10.2307/1374190
Brown, R. E. Bacula of some new world molossid bats. Mammalia 31(4), 645–667 (1967).
doi: 10.1515/mamm.1967.31.4.645
Brown, R. E., Genoways, H. H. & Jones, J. J. K. Bacula of some Neotropical bats. Mammalia 35(3), 456–464 (1971).
doi: 10.1515/mamm.1971.35.3.456
Sutton, D. A. The female genital bone of chipmunks, genus Eutamias. Southwestern Nat. 27, 393–402 (1982).
doi: 10.2307/3670714
Carosi, M., Spani, F., Ulland, A. E., Scalici, M. & Suomi, S. J. Clitoral length in immature and mature captive tufted capuchin (Sapajus spp.) females: A cross-sectional study. Am J Primatol. 82, e23135. https://doi.org/10.1002/ajp.23135 (2020).
doi: 10.1002/ajp.23135
pubmed: 32319142
pmcid: 7577954
Rau, A. S. & Hiriyannaiya, S. Contributions to our knowledge of the anatomy of the Lemuroidea. II. The urinogenital system of Loris lydekkerianus. J. Mysore Univ. 4, 1–19 (1930).
Hill, O. W. C. A monograph on the Genus Loris: With an account of the external, cranial and dental characters of the genus: A revision of the known forms, and the description of a new form from northern Ceylon. Ceylon J. Sci. 18(1), 89–132 (1933).
Clark, W. E. G. Early Forerunners of Man (Tindall & Cox, 1934).
Matthews, L. H. Notes on the genital anatomy and physiology of the gibbon (Hylobates). J. Zool. 116(2), 339–364 (1946).
Hill, O. W. C. Primates-Comparative Anatomy and Taxonomy (University Press, 1953).
Hill, O. W. C. & Davies, D. V. XVII-The reproductive organs in Hapalemur and Lepilemur. Proc. R. Soc. Edinb. B. 65(3), 251–270 (1954).
Hill, O. W. C. B. Vol. 3: External genitalia. In Primatologia (eds Hofer, H. et al.) 630–704 (Karger Publishers, 1958).
Petter-Rousseaux, A. Recherches sur la biologie de la reproduction de Primates inférieurs. Mammalia 26, 7–88 (1962).
Butler, H. The reproductive biology of a strepsirrhine (Galago senegalensis senegalensis). Int. Rev. Gen. Exp. Zool. 1, 241–296 (1964).
doi: 10.1016/B978-1-4831-9977-1.50012-2
Machida, H. & Giacometti, L. The anatomical and histochemical properties on the skin of the external genitalia of the primates. Folia Primatol. 6(1–2), 48–69 (1967).
doi: 10.1159/000155067
Groves, C. P. Vol. 1: Systematics and phylogeny of gibbons. In Gibbons and Siamang (ed. Rumbaught, D. M.) 1–89 (Karger Publishers, 1972).
Hill, O. W. C. Evolutionary Biology of Primates (Academic Press, 1972).
Stockley, P. The baculum. Curr. Biol. 22(24), R1032–R1033 (2012).
pubmed: 23257184
doi: 10.1016/j.cub.2012.11.001
Glucksmann, A. & Cherry, C. P. The hormonal induction of an os clitoridis in the neonatal and adult rat. J. Anat. 112, 223–231 (1972).
pubmed: 5077194
pmcid: 1271196
Murakami, R. A histological study of the development of the penis of wild-type and androgen-insensitive mice. J. Anat. 153, 223–231 (1987).
pubmed: 3429322
pmcid: 1261796
Perelman, P. et al. A molecular phylogeny of living primates. PLoS Genet. 7(3), e1001342. https://doi.org/10.1371/journal.pgen.1001342 (2011).
doi: 10.1371/journal.pgen.1001342
pubmed: 21436896
pmcid: 3060065
Arnold, C., Matthews, L. J. & Nunn, C. L. The 10KTrees website: A new online resource for primate phylogeny. Evol. Anthropol. 19, 114–118 (2010).
doi: 10.1002/evan.20251
IUCN. The IUCN Red List of Threarened Species. Version 2019-3 (2019). http://www.iucnredlist.org (Accessed February, 25th 2019).
Springer, M. S. et al. Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species supermatrix. PLoS ONE 7(11), e49521. https://doi.org/10.1371/journal.pone.0049521 (2012).
doi: 10.1371/journal.pone.0049521
pubmed: 23166696
pmcid: 3500307
Kumar, S., Stecher, G., Suleski, M. & Hedges, S. B. TimeTree: A resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34, 1812–1819 (2017).
pubmed: 28387841
doi: 10.1093/molbev/msx116
Bett, W. R. The os penis in man and beast. J. R. Soc. Med. 44, 433–434 (1951).
doi: 10.1177/003591575104400605
Bett, W. R. The os penis in man and beast. Ann. R. Coll. Surg. Engl. 10(6), 405–409 (1952).
pubmed: 14934010
pmcid: 2377501
Eglitis, J. A. Occurrence of bone tissue in the human penis. J. Urol. 70(5), 749–758 (1953).
pubmed: 13109930
doi: 10.1016/S0022-5347(17)67980-1
Sarma, D. P. & Weilbaecher, T. G. Human os penis. Urology 35(4), 349–350 (1990).
pubmed: 2108520
doi: 10.1016/0090-4295(90)80163-H
Champion, R. H. & Wegrzyn, J. Congenital Os penis. J. Urol. 91(6), 663–664 (1964).
pubmed: 14172255
doi: 10.1016/S0022-5347(17)64197-1
Ruth, E. B. The os priapi: A study in bone development. Anat. Rec. 60(2), 231–249 (1934).
doi: 10.1002/ar.1090600209
Napier, J. R. & Napier, P. H. The Natural History of the Primates (British Museum of Natural History and Cambridge University Press, 1985).
Dixson, A. Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes, and Human Beings (Oxford University Press, 1998).
Woollard, H. H. The anatomy of Tarsius spectrum. J. Zool. 95, 1071–1184 (1925).
Hill, O. W. C. Primates—Comparative Anatomy and Taxonomy (Edinburgh University Press, 1955).
Hill, O. W. C. Observations on the genitalia of the Woolly Monkey (Lagothrix). J. Zool. 122, 973–984 (1953).
ITIS. Integrated Taxonomic Information System. Version 2020 (2020). http://www.itis.gov (Accessed February 24, 2020).
Burt, W. H. Bacula of north american mammals (University of Michigan Press, 1960).
doi: 10.3998/mpub.9690254
Patterson, B. D. & Thaeler, C. S. The mammalian baculum: Hypotheses on the nature of bacular variability. J. Mammal. 63(1), 1–15 (1982).
doi: 10.2307/1380665
Wilson, M. I. A note on the external genitalia of female squirrel monkeys (Saimiri sciureus). J. Med. Primatol. 6, 181–185 (1977).
pubmed: 410941
doi: 10.1159/000459741
Cooper, N. et al. Sex biases in bird and mammal natural history collections. Proc. R. Soc. B 286(1913), 2019–2025 (2019).
doi: 10.1098/rspb.2019.2025
Gower, G. et al. Widespread male sex bias in mammal fossil and museum collections. Proc. Natl. Acad. Sci. U.S.A. 116(38), 19019–19024 (2019).
pubmed: 31481609
pmcid: 6754617
doi: 10.1073/pnas.1903275116
Jakovlić, I. The missing human baculum: A victim of conspecific aggression and budding self-awareness? Mamm. Rev. https://doi.org/10.1111/mam.12237 (2021).
doi: 10.1111/mam.12237
Spani, F., Morigi, M. P., Bettuzzi, M., Scalici, M. & Carosi, M. A 3D journey on virtual surfaces and inner structure of Ossa genitalia in Primates by means of a non-invasive imaging tool. PLoS ONE 15(1), e0228131. https://doi.org/10.1371/journal.pone.0228131 (2020).
doi: 10.1371/journal.pone.0228131
pubmed: 31999734
pmcid: 6992188
Brassey, C. A., Gardiner, J. D. & Kitchener, A. C. Testing hypotheses for the function of the carnivoran baculum using finite-element analysis. Proc. R. Soc. B 285(1887), 20181473 (2018).
pubmed: 30232157
doi: 10.1098/rspb.2018.1473
pmcid: 6170803
Carosi, M., Scalici, M. & Linn, G. S. Baubellum (Os clitoridis). In The International Encyclopedia of Primatology (eds Fuentes, A. et al.) (Wiley, 2016).
Arendt, J. & Reznick, D. Convergence and parallelism reconsidered: What have we learned about the genetics of adaptation? Trends Ecol. Evol. 23(1), 26–32 (2008).
pubmed: 18022278
doi: 10.1016/j.tree.2007.09.011
Haldane, J. B. S. The Causes of Evolution (Princeton Science Library, 1932).
Simpson, G. G. The Meaning of Evolution (Yale University Press, 1952).
Hall, B. K. Homoplasy and homology: Dichotomy or continuum? J. Hum. Evol. 52(5), 473–479 (2007).
pubmed: 17434571
doi: 10.1016/j.jhevol.2006.11.010
Carosi, M. & Scalici, M. Baculum (Os Penis). In The International Encyclopedia of Primatology (eds Fuentes, A. et al.) (Wiley, 2016).
Brassey, C. A., Behnsen, J. & Gardiner, J. D. Postcopulatory sexual selection and the evolution of shape complexity in the carnivoran baculum. Proc. R. Soc. B. 287(1936), 20201883. https://doi.org/10.1098/rspb.2020.1883 (2020).
doi: 10.1098/rspb.2020.1883
pubmed: 33049172
pmcid: 7657853
Bates, M. J. The design of browsing and berry-picking techniques for the online search interface. Online Rev. 13, 407–423 (1989).
doi: 10.1108/eb024320
Calvini, M., Siori, M. S., Gippoliti, S. & Pavia, M. Catalogue of the primatological collection of the Torino University. Nat. Hist. Sci. 3, 3–26 (2016).
doi: 10.4081/nhs.2016.286
Veracini, C., Ducci, L. & Agnelli, P. Review and historical notes on the non human primate collection of the Natural History Museum, Zoological Section «La Specola», Florence University, Italy. Atti Soc. Tosc. Sc. Nat. 117, 51–63 (2010).
Cracraft, J. Vl 1: Species concepts and speciation analysis. In Current Ornithology (ed. Johnston, R. F.) 159–187 (Springer, 1983).
doi: 10.1007/978-1-4615-6781-3_6
Rylands, A. B. & Mittermeier, R. A. Primate taxonomy: Species and conservation. Evol. Anthropol. 23(1), 8–10 (2014).
pubmed: 24591133
doi: 10.1002/evan.21387
Harrison, R. M. & Lewis, R. W. Vol. 3: The male reproductive tract and its fluids. In Comparative Primate Biology (eds Dukelow, W. R. & Erwin, J.) 101–148 (Wiley, 1986).
Hedges, S. B., Marin, J., Suleski, M., Paymer, M. & Kumar, S. Tree of life reveals clock-like speciation and diversification. Mol. Biol. Evol. 32(4), 835–845 (2015).
pubmed: 25739733
pmcid: 4379413
doi: 10.1093/molbev/msv037
Nielsen, R. Mapping mutations on phylogenies. Syst. Biol. 51, 729–739 (2002).
pubmed: 12396587
doi: 10.1080/10635150290102393
Huelsenbeck, J. P., Nielsen, R. & Bollback, J. P. Stochastic mapping of morphological characters. Syst. Biol. 52, 131–158 (2003).
pubmed: 12746144
doi: 10.1080/10635150390192780
Revell, L. J. Two new graphical methods for mapping trait evolution on phylogenies. Methods Ecol. Evol. 4(8), 754–759 (2013).
doi: 10.1111/2041-210X.12066
Revell, L. J. phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).
doi: 10.1111/j.2041-210X.2011.00169.x
Paradis, E. & Schliep, K. ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2019).
pubmed: 30016406
doi: 10.1093/bioinformatics/bty633
Pagel, M. Detecting correlated evolution on phylogenies: A general method for the comparative analysis of discrete characters. Proc. R. Soc. Lond. Biol. Sci. 255, 37–45 (1994).
doi: 10.1098/rspb.1994.0006
Fritz, S. A. & Purvis, A. Selectivity in mammalian extinction risk and threat types: A new measure of phylogenetic signal strength in binary traits. Conserv. Biol. 24(4), 1042–1051 (2010).
pubmed: 20184650
doi: 10.1111/j.1523-1739.2010.01455.x
R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria (2021). https://www.R-project.org . (Accessed February 23, 2019)