ARA Rev iew o fIf In terspec ific Hy bidibridiza tion in the Order Testudines

Timothy R. Brophy, Wayne Frair, and Darlene Clark Classification of Extant Turtles Order Testudines (Ernst et al., 2000) Suborder Pleurodira (side-necked turtles) FamilyPelomedusidae - S.A. & Africa Family Chelidae - S.A. & Australia Suborder Crytodira (hidden -necked turtles) Superfamily Trionychoidea FilKitFamily Kinostern idae - Md&MMud & Musk Family Dermatemydidae - C.A. River FilCtthlidFamily Carettochelyidae - Pig N ose Family Trionychidae - Softshell Classification of Extant Turtles Suborder Crytodira (hidden-necked turtles) Superfamily Chelonioidea Family Cheloniidae - Marine Family Dermochelyidae - Leatherback SSpuperfamily yT Testudinoidea Family Chelydridae - Snapping Family Platysternidae - Big Headed Family Emydidae - N.W. Pond Family Geoemydidae - OWO.W. Pond Family Testudinidae - Tortoises TTBurtle Baraminology

• Turtles have been the subject of much baraminological research (see Wood, 2005)

– Frair (1984) – All turtle species constitute a ppyypolytypic baramin with four diversification lines (Pleurod ira, Ch el onioid ea, T rionych id ae & rest of Cryptodira). Diversification line ≈ holobaramin

– Frair (1991) – All turtles descended from a created ancestor (possibl y PPgroganoche y ys))D. Did not discard hypothesis of four diversification lines TTBurtle Baraminology

• Turtles have been the subject of much baraminological research (see Wood, 2005)

– Wise (1992) – Turtles are apobaraminic. Some evidence supports Frair’s (1984) four holobaramins

– Robinson (1997) – Further supports contention tha t tur tles are apo baram in ic. Che lon iidae & Gopherus are monobaraminic Turtle Baraminology

• Turtles have been the subject of much baraminological research (see Wood , 2005)

– WW(5)ood (2005) – TTpurtles are apobaraminic

– Composed of five holobaramins: Chelidae, Pelomedusidae, Trionychoidea, other Cryptodira & Proganochelys TTHyurtle Hybridization

• AAg thorough review of inters pecific hybridization, with baraminological interppypretations, has yet to be reported

• Robinson (1997) incorporated the use of hbiditihybridization in hibhis baram ino log ica l ana lyses o f the marine turtles & gopher tortoises

• We set out to find evidence of interspecific hyygbridization throughout the entire turtle order & use this evidence to “build” monobaramins SSyRummary of Results

• EEyvidence of hybridization in 8 of 1 3 families

Pelomedusidae Chelidae Kinosternidae

DDyermatem1ydidae CCyarrettochel1 yidae TTyrionychidae Cheloniidae Dermochelyidae1 Chelydridae Platysternidae1

Emydddidae GddGeoemydidae TddTestudinidae Summary of Results

• Crosses between 89 unique species pairs

• 29 of these are intergeneric (≈33%)

• No interfamilial or inter-holobaraminic ((W,5)sensu Wood, 2005) crosses

• 16 small monobaramins (2-4 species)

• 2 medium monobaramins (5-8 species)

• 2 large monobaramins (>8 species) FFyPamily Pelomedusidae – 1sm.

1 cross 2 spp.

Pelusios seychellensis Pelusios castanoides

1 Small Monobaramin FFyCamily Chelidae – 2sm.

3 crosses Chelodina longicollis 2IG2 IG 4 spp.

1st Small Monobaramin

Chelodina canni

Emydura Elseya albertisii novaeguineae FFyCamily Chelidae

Phrynops hilari s

3 crosses 4spp4 spp. Phrynops geoffroanu

Phrynops williamsi williamsi Phrynops gibbus 2nd Small Monobaramin Family Kinosternidae – 1med.

itb bKi t nosternon subrubrum Ki fl t nosternon flavescens Kinosternon baurii

Sternotherus depressus Sternotherus carinatus

6 crosses Sternotherus minor Sternotherus odoratus 1 IG 7 spp. 1 Medium Monobaramin FFyTyamily Trionychidae – 1sm.

1 “cross” 2 spp.

Apalone spinifera Apalone mutica

1 Small Monobaramin Family Cheloniidae – 1med.

7 crosses 6 IG, 3 IT 5 spp.

Lepidochelys kempii Lepidochelys olivacea

Caretta carettacaretta

1M1 Medi um M onob arami n

Eretmochelys imbricata Chelonia mydas FFyCamily Cheloniidae

• What about NNp(atator depressus (flatback turtle ))?

and New Guinea (Karl et al., 1995)

• No records records of of hybridization hybridization with with any any other other species species

• May be be due due in partin part to its to limited its limited range range in Australia in Australia Family Cheloniidae

• Tribes Carettini (Caretta, Lepidochelys & Er tmochetmoch lyselys)&Ch) & Che lonini (Ch loniaelonia) thought to have been separated for 50-75 million years

• “May be among the oldest vertebrate lineages capppable of producing viable hy brids in nature” (Kar l et a l., 1995 ) Baraminology of the Cheloniidae

• Robinson (1997) considered the Cheloniidae in his baram ino log ica l ana lyses: – Concluded entire family was a single monobaramin – NttNatator d depressus fllithifell within ran ge o f cy toc hrome b sequence variation of hybridizing turtles, so it was included as part of the monobaramin • We reviewed several recent reports of hyyyCbridization in the family Cheloniidae – Published since or not included in Robinson (1997) – Several with molecular verification – Confirm Robinson’s (1997) conclusions Recent Reports of Sea Turtle Hybridization

Species Crossed N/A? Evidence Reference

Morphology, Caretta caretta x Lepidochelys kempii Natural mtDNA Barber et al., 2003 & nuclear DNA

Morphology, Garman, 1888; Caretta caretta x Eretmochelys imbricata Natural mtDNA Kamezaki, 1983; Frazier, 1988; & nuclear DNA Witzell & Schmid, 2003

Kamezake et al., 1996; Morphology & Hemens, 1997; Kawata, 2003; Caretta caretta x Chelonia mydas Natural mtDNA Phillips, 2003; Jones et al., 2004

Morphology, Buden & Edward, 2001; Chelonia mydas x Eretmochelys imbricata Natural mtDNA Kawata, 2003; & scnDNA Seminoff et al., 2003 Family Testudinidae – 6sm.

Testudo graeca Testudo hermanni

3 crosses 4 spp.

Testudo horsfieldi horsfieldi Testudo marginata marginata 1st Small Monobaramin FFyTamily Testudinidae

1 cross 2 spp.

Indotestudo forstenii Indotestudo elongata

2nd SllMbSmall Monobaramin FFyTamily Testudinidae

1 cross 2 spp.

Gopherus berlandieri Gopherus agassizii

3rd SllMbSmall Monobaramin Baraminology of Gopher Tortoises

• Robinson (1997) considered the genus Gopherus in his baraminological analyses:

– Concluded entire genus was a single monobaramin (4 spp)ecies): G. agg,assizii, G. , berlandieri, G. flavomarginatus, G. polyphemus

– G. flavomarginatus flavomarginatus & & G. G. polyphemus polyphemus fell within range of cytochrome b sequence variation of hybridizing turtles, so they were included as part of the monobaramin Family Testudinidae

Kinixys erosa

3 crosses 3 spp. Kinixys homeana 4th Small Monobaramin

Kinixys belliana Family Testudinidae Madagascar SAmericaS. America

Geochelone denticulata denticulata GhlGeochelone ra ddiata 2 crosses, 3 spp.

GhlGeochelone car bbonaria ??? 1 cross, 2 spp.

Geochelone sulcata 5th & 6th Small Monobaramins

Geochelone pardalis EdidEdiEmydidae: Emydinae – 3sm.

1 cross 2 spp.

TlTerrapene carolina Terrapene ornata

1st Small Monobaramin Fam ily Emy didae: Emy dinae

1cross1 cross 1 IG Clemmys guttata Glyptemys muhlenbergii2 spp.

2nd SllMbSmall Monobaramin Familyyy Emydidae: Em ydinae Glyptemys insculpta

4 crosses Emys blandingii 4 IG 4 spp.

Emys Actinemys orbicularis marmorata 3rd Small Monobaramin Wood x Blandinggy’s Hybrid

X Hybridization in the Emydinae • Emydinae = Clemmys, Glyptemys, Actinemys, Emys & Terrapene

Clemmysguttata guttata Glyptemys spp.

Terrapene spp.

1 Large Monobaramin?

Actinemys marmorata Emys spp. Emydidae: Deirochelyinae - 1sm.&1l.

Trachemys stejnegeri

2 crosses 3 spp.

ThTrachemys d decorata ThTrachemys terrapen 1 Small Monobaramin P. floridana FamilyP. alabamensis Emydidae: Deirochelyinae P. concinna

P. rubriventris

C. picta P. nelsoni P. texana

GGp. p gsuedo g p geographica TTp. scripta

G. versa GhitiG. ouachitensis G. barbouri

G. kohnii GhiG. geographica

G. nigrinoda

G. oculifera Hybridization in the Deirochelyinae • Deirochelyinae = Graptemys, Trachemys, Chrysemys, Psuedemys, Malaclemys & Deirochelys

21 crosses Trachemys scripta spp. 5 IG 16 spp.

Graptemys 1 Large

Pseudemys spp. Monobaramin Chrysemys picta Family Geoemydidae – 2sm.&1l.

Rhinoclemmys punctularia

3 crosses 3 spp. h lRhi l noclemmys melanosterna Rhi di td l noclemmys diademata 1st Small Monobaramin FilGFamily Geoemy didae

1 cross 2 spp.

Mauremys Mauremyscaspica rivulata

2nd SllMbSmall Monobaramin M. japonica M. mutica Family Geoemydidae M. reevesii

M. annamensis

Mal.M. nigricans subtri

M. sinensis H. grandis

R. Pulcherimma S. pseudocellata (C. America)

C. galbinifrons juga Cyc.G. japonica shanensis

S. quadriocellata CbiC. amboinensis i CflC. fl iavomarginata

C. mouhotii C. bourreti C. trifasciata Heosemys grandis Hybridization in the Geoemydidae 26 crosses, 11 IG, 19 species

Mauremys

* Geoemyda japonica

Cyclemys shanensis

Rhinoclemmys pulcherimma spp. Cuora spp.

Sacalia spp.

1 Large Monobaramin *Large phylogenetic distance Malayemys subtrijuga Proposed Phylogeny ofhf the Geoemyd ddidae

*

* Spinks et al., 1994 Discussion • 288 turtle species – 41,238 possible hybrids (0.22%) – 5,971 possible intra-fllhbd()familial hybrids (1.5%) • GGgrowing turtle monobaramins – Continue to verify records we already have – MMy,y,any, as yet, undescribed & undiscovered h ybrids (many in process of being published) – Inclusion of non-hybridizing turtles if they fall within range offhbdlf variation of hybridizing turtles • WWjW(5)e are unable to reject Wood’s (2005) hypothesis of five turtle holobaramins