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AR I Fi T Ifi H Bidi Ti a Review of Interspecific Hybridization in the Order Testudines

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AR I Fi T Ifi H Bidi Ti a Review of Interspecific Hybridization in the Order Testudines 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 Nose 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 (Pleuro dira, Ch el onioi dea, T rionych id ae & rest of Cryptodira). Diversification line ≈ holobaramin – Frair (1991) – All turtles descended from a created ancestor (possibly PPgroganocheys y))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 Chelodina canni 4 spp. 1st Small Monobaramin Emydura albertisii Elseya novaeguineae FFyCamily Chelidae Phrynops hilari Phrynops geoffroanus 3 crosses 4spp4 spp. Phrynops williamsi Phrynops gibbus 2nd Small Monobaramin Family Kinosternidae – 1med. Kinos ternon su bru brum Kinos ternon 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 caretta 1M1 Medi um M onob arami n Eretmochelys imbricata Chelonia mydas FFyCamily Cheloniidae • What about NNp(atator depressus (flatback turtle ))? • No records of hybridization with any other species • May be due in part to its limited range in Australia and New Guinea (Karl et al., 1995) Family Cheloniidae • Tribes Carettini (Caretta, Lepidochelys & Ere tmoche lys)&Ch) & Chelonini (Che lonia) 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 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 Testudo 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 & G. 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 Kinixys belliana 4th Small Monobaramin Family Testudinidae Madagascar SAmericaS. America Geochelone denticulata GhldGeochelone radiata 2 crosses, 3 spp. GhlGeochelone car bonaria ??? 1 cross, 2 spp. Geochelone sulcata Geochelone pardalis 5th & 6th Small Monobaramins 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 guttata2 spp. Glyptemys muhlenbergii 2nd SllMbSmall Monobaramin Familyyy Emydidae: Em ydinae Glyptemys insculpta 4 crosses Emys blandingii 4 IG 4 spp. Emys orbicularis Actinemys marmorata 3rd Small Monobaramin Wood x Blandinggy’s Hybrid X Hybridization in the Emydinae • Emydinae = Clemmys, Glyptemys, Actinemys, Emys & Terrapene Clemmys guttata Glyptemys spp. Terrapene spp. 1 Large Monobaramin? Actinemys marmorata Emys spp. Emydidae: Deirochelyinae - 1sm.&1l. Trachemys stejnegeri 2 crosses 3 spp. ThTrachemys decorata ThTrachemys terrapen 1 Small Monobaramin Family Emydidae: Deirochelyinae P. floridana P. concinna P. rubriventris P. alabamensis P. texana C. picta P. nelsoni GGp. psuedog eog rap hica TTp. scripta G. versa GhitiG. ouachitensis G. kohnii GhiG. geographica G. barbouri G. oculifera G. nigrinoda Hybridization in the Deirochelyinae • Deirochelyinae = Graptemys, Trachemys, Chrysemys, Psuedemys, Malaclemys & Deirochelys 21 crosses Trachemys scripta Graptemys spp. 5 IG 16 spp. 1 Large Pseudemys spp. Monobaramin Chrysemys picta Family Geoemydidae – 2sm.&1l. Rhinoclemmys punctularia 3 crosses 3 spp. Rhinoc lemmys me lanosterna Rhinoc lemmys dia dema tta 1st Small Monobaramin FilGFamily Geoemy didae 1 cross 2 spp. Mauremys caspica Mauremys rivulata 2nd SllMbSmall Monobaramin Family Geoemydidae M. japonica M. reevesii M. annamensis M. mutica M. sinensis M. nigricans Cyc. shanensis H. grandis S. quadriocellata R. Pulcherimma S. pseudocellata (C. America) Mal. subtrijuga G. japonica CbiiC. amboinensis CflC. flavomarg inata C. galbinifrons C. mouhotii C. bourreti C. trifasciata Hybridization in the Geoemydidae 26 crosses, 11 IG, 19 species Heosemys grandis * Geoemyda japonica Cyclemys shanensis Mauremys spp. Cuora spp. Sacalia spp. 1 Large Monobaramin Rhinoclemmys pulcherimma *Large phylogenetic distance Malayemys subtrijuga Proposed Phylogeny ofhf the Geoemy dddidae * * 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.
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