Fossil constraints on the origin and evolution of Platyhelminthes are surprisingly concordant with modern molecular phylogenies

De Baets, Kenneth; Dentzien-Dias, Paula; Huntley, John Warren; Vanhove, Maarten P.M.; Łaska, Weronika; Skawina, Aleksandra; Steenkiste, Niels W.L. Van; Vanadzina, Karina

doi:10.1590/S1984-4689.v41.e24002

person Kenneth De Baets

Conceptualization · Funding acquisition · Investigation · Methodology · Project administration · Supervision · Validation · Visualization · Writing - original draft · Writing - review & editing

schoolInstitute of Evolutionary Biology, Faculty of Biology, University of Warsaw. ul. Żwirki i Wigury 101, 02-089 Warszawa, Poland.

0000-0002-1651-321X

person Paula Dentzien-Dias

Investigation · Methodology · Validation · Writing - original draft · Writing - review & editing

schoolInstituto de Geociências, Departamento de Paleontologia e Estratigrafia, Universidade Federal do Rio Grande do Sul. Avenida Bento Gonçalves 9500, 91501-970 Porto Alegre, RS, Brazil.

0000-0001-8708-6799

person John Warren Huntley

Investigation · Methodology · Validation · Visualization · Writing - original draft · Writing - review & editing

schoolDepartment of Geological Sciences, University of Missouri. Columbia, MO 65211, USA.

0000-0001-9955-8853

person Maarten P.M. Vanhove

Investigation · Methodology · Validation · Writing - original draft · Writing - review & editing

schoolHasselt University, Centre for Environmental Sciences, Research Group Zoology: Biodiversity & Toxicology. Agoralaan Gebouw D, 3590 Diepenbeek, Belgium.

0000-0003-3100-7566

person Weronika Łaska

Investigation · Methodology · Validation · Writing - original draft · Writing - review & editing

schoolInstitute of Evolutionary Biology, Faculty of Biology, University of Warsaw. ul. Żwirki i Wigury 101, 02-089 Warszawa, Poland.

0000-0001-5034-5240

person Aleksandra Skawina

Investigation · Methodology · Validation · Visualization · Writing - original draft · Writing - review & editing

schoolInstitute of Evolutionary Biology, Faculty of Biology, University of Warsaw. ul. Żwirki i Wigury 101, 02-089 Warszawa, Poland.

0000-0002-8287-1568

person Niels W.L. Van Steenkiste

Investigation · Methodology · Validation · Writing - original draft · Writing - review & editing

schoolDepartments of Botany and Zoology, University of British Columbia. Vancouver, BC, V6T 1Z4, Canada.

0000-0002-2676-7862

person Karina Vanadzina

Conceptualization · Investigation · Methodology · Validation · Visualization · Writing - original draft · Writing - review & editing

schoolInstitute of Evolutionary Biology, Faculty of Biology, University of Warsaw. ul. Żwirki i Wigury 101, 02-089 Warszawa, Poland.

0000-0002-7952-2658

Corresponding author: Kenneth De Baets (
kenneth.debaets@gmail.com)

Editorial responsibility

Fernando Carbayo

Competing Interests

The authors have declared that no competing interests exist.

Node	Min. Age (Ma)	Stratigraphy, Stage, Country	Coll.	Environment	Support	Reference
Platyhelminthes (free-living turbellarians)	444.0	Vauréal Fm., Katian, Canada	MfN	Marine	Characteristic trails	Knaust and Desrochers (2019)
Tricladida	274.4	Pizzo del Diavolo Fm., Kungurian, Italy	MNHN	Freshwater	Characteristic trails	Alessandrello et al. (1988)
Monopisthocotylea	377.7	Lode Fm., Givetian, Latvia	LDM	Marginal marine	Circlets with up to 16 hooks	Upeniece (2001)
Cestoda	304.8	Stark Shale Mb., Kasimovian, USA	PF	Marine	Egg with similar surface ornamentation and size	Zangerl and Case (1976)
Eucestoda	259.1	Rio do Rasto Fm., Wordian-Capitanian, Brazil	UFRGS	Freshwater	Egg arranged in proglottids	Dentzien-Dias et al. (2013)
Trematoda	120.2	La Huérguina Fm., Barremian, Spain	MUPA	Freshwater	Egg with operculum	Barrios-de Pedro et al. (2020)
Gymnophallidae	75.22	Judith River Fm., Campanian, USA	UC	Freshwater	Characteristic igloo-shaped concretion	Rogers et al. (2018)
Gymnophallidae	52.93	London Clay Fm., Ypresian, England	NHM	Marine	Characteristic pit with raised rime	Todd and Harper (2011)

Age (yrs BP)	Site	Site ID (Map)	Family	Taxonomic unit identified	Source	Type of find	Putative host	Reference
Pleistocene
550 000	Caune de l’Arago Cave, France	a	Dicrocoeliidae	Dicrocoeliidae	Coprolites	Parasite eggs	Carnivorous mammal	Jouy-Avantin et al. (1999)
16 985¹	Cueva Huenul 1, Argentina	b	Anoplocephalidae	Viscachataenia quadrata	Coprolites	Parasite eggs	Rodent	Beltrame et al. (2012)
12 680²	Cueva del Milodón, Chile	c	Hymenolepididae	Hymenolepididae	Coprolites	Parasite eggs	Mylodon darwini (Darwin’s ground sloth)	Oyarzún-Ruiz et al. (2021)
			Taeniidae	Taeniidae
Holocene
10 421³	Cerro Casa de Piedra 7, Argentina	1	Anoplocephalidae	Anoplocephalidae	Coprolites	Parasite eggs	Human	Fugassa et al. (2010)
			Hymenolepididae	Rodentolepis sp.
10 049	East Chia Sabz, Iran	2	Taeniidae	Taeniidae	Sediment from skeletal remains	Parasite eggs	Canid	Paknezhad et al. (2017)
10 000⁴	Coast, Peru	3	Diphyllobothriidae	Adenocephalus pacificus	Mummified remains	NS	Human	Reinhard and Barnum (1991) in: Reinhard (1992)
9 549⁵	Shillourokambos, Cyprus	4	Fasciolidae	Fasciola hepatica	Sediment from skeletal remains	Parasite eggs	Human	Harter-Lailheugue et al. (2005)
8 949	Zamostye 1,2, Russia	5	Diplostomidae	Alaria alata	Coprolites	Parasite eggs	Canid	Engovatova and Khrustalev (1996) in: Slepchenko and Reinhard (2018)
			Opisthorchiidae	Opisthorchis felineus
7 849	Atacama, Chile	6	Troglotrematidae	Paragonimus sp.	Coprolites	Parasite eggs	Human	Hall (1976) in: Horne (1985)
7 315⁶	Euphrates Cave, New Zealand	7	Notocotylidae	Notocotylidae	Coprolites	DNA trace	Moa	Boast et al. (2018)
7 26⁹7	La Draga, Spain	8	Dicrocoeliidae	Dicrocoelium dendriticum	Sediment from occupational layers	DNA trace	Ruminant	Maicher et al. (2017)
			Paramphistomidae	Paramphistomum
6 500⁸	Tell Zeidan, Syria	9	Schistosomatidae	Schistosoma sp.	Sediment from skeletal remains	Parasite eggs	Human	Anastasiou et al. (2014)
5 125	Zürich-Parkhaus-Opéra, Switzerland	10	Echinostomatidae	Echinostoma	Sediment from occupational layers	Parasite eggs	Mammal or bird	Maicher et al. (2019)
3 059	Tarapacá-40, Chile	11	Dipylidiidae	Dipylidium caninum	Mummified remains	Parasite eggs	Human	Ramirez et al. (2021)
1 726⁹	Chehrabad Salt Mine, Iran	12	Davaineidae	Fuhrmannetta malakartis	Coprolites	DNA trace	Bird	Askari et al. (2022)
1 600¹⁰	St Lawrence Island, USA	13	Heterophyidae	Cryptocotyle lingua	Mummified remains	Parasite Eggs	Human⁵	Zimmerman and Smith (1975)
449	Sapgyo, South Korea	14	Gymnophallidae	Gymnophalloides seoi	Mummified remains	Parasite Eggs	Human	Shin et al. (2012)

¹
Based on calibrated radiocarbon age estimates for stratigraphic unit VII of Cueva Huenul 1 in Tietze et al. (2019): 13 844 ± 75 yrs BP (16 390 - 16 985 cal yrs BP).
²
Earliest radiocarbon age estimate for Cueva del Milodón from Borrero et al. (1999): 12 552 ± 128 yrs BP.
³
Based on calibrated radiocarbon age estimates for archaeological layer XVI of CCP7 in Velázquez et al. (2014): 8 920 ± 200 yrs BP (9 495 - 10 421 cal yrs BP).
⁴
Due to the lack of further details associated with this finding, the next earliest finding of Diphyllobothriidae was from Shillourokambos sediment sample (see the next row), reported in Le Bailly and Bouchet (2013).
⁵
The PhD thesis by the first author (Harter 2003) provides an earlier date for the burial containing remains of Taeniidae and Fasciolidae (10 449 BP or 8 500 BC).
⁶
Based on the earliest calibrated radiocarbon age estimates for Euphrates Cave in Wood et al. (2012): 6 368 ± 31 yrs BP; 7 315 - 7 165 cal yrs BP. Wood et al. 2013 also found a DNA trace of a sister family to Notocotylidae in coprolites of similar age deposited by extinct New Zealand moa.
⁷
Another find of dicrocoeliid eggs close in age was obtained from sediment from a domestic context, Leipzig-Zwenkau, Germany, 7 208 yrs BP (5 259 yrs BC) reported in Le Bailly and Bouchet (2010).
⁸
Schmidt et al. 1992 reported ‘schistosome-like’ eggs - but without the characteristic operculum - in dung balls of Nothrotheriops shastensis (Shasta ground sloth) from Rampart Cave, Arizona, USA, radiocarbon dated at 10 500 ± 180 yrs BP.
⁹
The earliest date corresponds to the establishment of Sassanid Empire (224-651 AD), Askari et al. (2018).
¹⁰
Considered to be a case of ‘false parasitism’: an incidental finding of a parasite in a species that is not normally part of its lifecycle. In this case, the human was thought to have consumed fish infected by Cryptocotyle lingua.

[TFN1] ¹
Based on calibrated radiocarbon age estimates for stratigraphic unit VII of Cueva Huenul 1 in Tietze et al. (2019): 13 844 ± 75 yrs BP (16 390 - 16 985 cal yrs BP).

[TFN2] ²
Earliest radiocarbon age estimate for Cueva del Milodón from Borrero et al. (1999): 12 552 ± 128 yrs BP.

[TFN3] ³
Based on calibrated radiocarbon age estimates for archaeological layer XVI of CCP7 in Velázquez et al. (2014): 8 920 ± 200 yrs BP (9 495 - 10 421 cal yrs BP).

[TFN4] ⁴
Due to the lack of further details associated with this finding, the next earliest finding of Diphyllobothriidae was from Shillourokambos sediment sample (see the next row), reported in Le Bailly and Bouchet (2013).

[TFN5] ⁵
The PhD thesis by the first author (Harter 2003) provides an earlier date for the burial containing remains of Taeniidae and Fasciolidae (10 449 BP or 8 500 BC).

[TFN6] ⁶
Based on the earliest calibrated radiocarbon age estimates for Euphrates Cave in Wood et al. (2012): 6 368 ± 31 yrs BP; 7 315 - 7 165 cal yrs BP. Wood et al. 2013 also found a DNA trace of a sister family to Notocotylidae in coprolites of similar age deposited by extinct New Zealand moa.

[TFN7] ⁷
Another find of dicrocoeliid eggs close in age was obtained from sediment from a domestic context, Leipzig-Zwenkau, Germany, 7 208 yrs BP (5 259 yrs BC) reported in Le Bailly and Bouchet (2010).

[TFN8] ⁸
Schmidt et al. 1992 reported ‘schistosome-like’ eggs - but without the characteristic operculum - in dung balls of Nothrotheriops shastensis (Shasta ground sloth) from Rampart Cave, Arizona, USA, radiocarbon dated at 10 500 ± 180 yrs BP.

[TFN9] ⁹
The earliest date corresponds to the establishment of Sassanid Empire (224-651 AD), Askari et al. (2018).

[TFN10] ¹⁰
Considered to be a case of ‘false parasitism’: an incidental finding of a parasite in a species that is not normally part of its lifecycle. In this case, the human was thought to have consumed fish infected by Cryptocotyle lingua.