ar i fi t ifi h b idi tia review of interspecific

A R i f I t ifi H b idi tiA Review of Interspecific Hybridization in the Order Testudines

Timothy R. Brophy,Wayne Frair, and Darlene Clark

Classification of Extant TurtlesOrder Testudines (Ernst et al., 2000)

Suborder Pleurodira (side-necked turtles)FamilyPelomedusidae - S.A. & AfricaFamily Chelidae - S.A. & Australia

Suborder Crytodira (hidden-necked turtles)Suborder Crytodira (hidden necked turtles)Superfamily Trionychoidea

F il Ki t id M d & M kFamily Kinosternidae - Mud & MuskFamily Dermatemydidae - C.A. RiverF il C tt h l id Pi NFamily Carettochelyidae - Pig NoseFamily Trionychidae - Softshell

Classification of Extant TurtlesSuborder Crytodira (hidden-necked turtles)

Superfamily ChelonioideaFamily Cheloniidae - MarineFamily Dermochelyidae - Leatherback

Superfamily TestudinoideaS p y TFamily Chelydridae - SnappingFamily Platysternidae - Big HeadedFamily Platysternidae Big HeadedFamily Emydidae - N.W. PondFamily Geoemydidae - O W PondFamily Geoemydidae O.W. PondFamily Testudinidae - Tortoises

Turtle BaraminologyT B gy

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

– Frair (1984) – All turtle species constitute a polytypic baramin with four diversification lines (Pl d Ch l d T h d fp y yp(Pleurodira, Chelonioidea, Trionychidae & rest of Cryptodira). Diversification line ≈ holobaramin

– Frair (1991) – All turtles descended from a created ancestor (possibly Proganocheys). Did not discard (p y P g y ) Dhypothesis of four diversification lines

Turtle BaraminologyT B gy

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

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

– Robinson (1997) – Further supports contention th t t tl b i i Ch l iid &that turtles are apobaraminic. Cheloniidae & Gopherus are monobaraminic

Turtle BaraminologyTurtle Baraminology

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

– Wood (2005) – Turtles are apobaraminicW ( 5) T p

– Composed of five holobaramins: Chelidae, pPelomedusidae, Trionychoidea, other Cryptodira & Proganochelys

Turtle HybridizationT Hy• A thorough review of interspecific A g p

hybridization, with baraminological interpretations, has yet to be reportedp y p

• Robinson (1997) incorporated the use of h b idi ti i hi b i l i l l fhybridization in his baraminological analyses of the marine turtles & gopher tortoises

• We set out to find evidence of interspecific hybridization throughout the entire turtle order y g& use this evidence to “build” monobaramins

Summary of ResultsS y R• Evidence of hybridization in 8 of 13 familiesE y 3

Pelomedusidae Chelidae Kinosternidae

Dermatemydidae Carrettochelyidae Trionychidae1 1D y C y T y

Cheloniidae Dermochelyidae Chelydridae Platysternidae

11

11Cheloniidae Dermochelyidae Chelydridae Platysternidae

d d G d d T d d

11Emydidae Geoemydidae Testudinidae

Summary of Results• Crosses between 89 unique species pairs

• 29 of these are intergeneric (≈33%)

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

• 16 small monobaramins (2-4 species)p

• 2 medium monobaramins (5-8 species)

• 2 large monobaramins (>8 species)

Family Pelomedusidae – 1sm.F y P

1 cross 2 spp.

Pelusios seychellensis Pelusios castanoides

1 Small Monobaramin

Family Chelidae – 2sm.F y C

3 crosses 2 IGChelodina longicollis Chelodina canni2 IG

4 spp.

1st Small Monobaramin

Emydura albertisii Elseya novaeguineae

Family ChelidaeF y C

Phrynops hilari Phrynops geoffroanus

3 crosses 4 spp

Phrynops williamsi

4 spp.

Phrynops williamsiPhrynops gibbus

2nd Small Monobaramin

Family Kinosternidae – 1med.

Ki t flKi t b b Kinosternon flavescensKinosternon subrubrumKinosternon baurii

Sternotherus carinatusSternotherus depressus

Sternotherus minor Sternotherus odoratus6 crosses

1 Medium Monobaramin1 IG

7 spp.

Family Trionychidae – 1sm.F y T y1 “cross”

22 spp.

Apalone spinifera Apalone mutica

1 Small Monobaramin

Family Cheloniidae – 1med.7 crosses 6 IG, 3 IT

Lepidochelys olivaceaLepidochelys kempii

5 spp.

Caretta caretta

1 M di M b i

Caretta caretta

1 Medium Monobaramin

Chelonia mydasEretmochelys imbricata

Family CheloniidaeF y C• What about Natator depressus (flatback turtle)?W N p ( )

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

• May be due in part to its limited range in Australia• May be due in part to its limited range in Australia and New Guinea (Karl et al., 1995)

Family CheloniidaeFamily Cheloniidae

• Tribes Carettini (Caretta, Lepidochelys & Eretmochelys) & Chelonini (Chelonia) thought toEr tmoch lys) & Ch lonini (Ch lonia) thought to have been separated for 50-75 million years

• “May be among the oldest vertebrate lineages capable of producing viable hybrids in nature” (K l l )

p p y(Karl et al., 1995)

Baraminology of the Cheloniidaegy• Robinson (1997) considered the Cheloniidae in

hi b i l i l lhis baraminological analyses:– Concluded entire family was a single monobaramin

N t t d f ll ithi g f t h b– Natator depressus fell within range of cytochrome b sequence variation of hybridizing turtles, so it was included as part of the monobaramin

• We reviewed several recent reports of hybridization in the family Cheloniidaey y C– 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

Caretta caretta x Lepidochelys kempii NaturalMorphology,

mtDNA& nuclear DNA

Barber et al., 2003

Caretta caretta x Eretmochelys imbricata NaturalMorphology,

mtDNA& nuclear DNA

Garman, 1888;Kamezaki, 1983; Frazier, 1988;

Witzell & Schmid, 2003

Caretta caretta x Chelonia mydas Natural Morphology & mtDNA

Kamezake et al., 1996; Hemens, 1997; Kawata, 2003;

Phillips 2003;mtDNA Phillips, 2003;Jones et al., 2004

Morphology, Buden & Edward, 2001;Chelonia mydas x Eretmochelys imbricata Natural

Morphology, mtDNA

& scnDNA

Buden & Edward, 2001;Kawata, 2003;

Seminoff et al., 2003

Family Testudinidae – 6sm.y

Testudo graeca Testudo hermanni

3 crosses

Testudo horsfieldi Testudo marginata

4 spp.

Testudo horsfieldi Testudo marginata


Family TestudinidaeF y T

1 cross 2 spp.

Indotestudo forstenii Indotestudo elongata

d S ll M b2nd Small Monobaramin

Family TestudinidaeF y T

1 cross 2 spp.

Gopherus berlandieri Gopherus agassiziip p

d S ll M b3rd Small Monobaramin

Baraminology of Gopher TortoisesBaraminology of Gopher Tortoises

• Robinson (1997) considered the genus Gopherusin his baraminological analyses:– Concluded entire genus was a single monobaramin (4

species): G. agassizii, G. berlandieri, p ) g , ,G. flavomarginatus, G. polyphemus

– G. flavomarginatus & G. polyphemus fell within range ofG. 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 belliana4th Small Monobaramin

pp

Family TestudinidaeMadagascar S AmericaMadagascar S. America

Geochelone denticulataG h l d Geochelone denticulata

G h l b

Geochelone radiata2 crosses, 3 spp.

Geochelone carbonaria

???1 cross, 2 spp.

5th & 6th Small MonobaraminsGeochelone sulcata Geochelone pardalis

E did E di 3Emydidae: Emydinae – 3sm.

1 cross 2 spp.pp

T l TTerrapene carolina Terrapene ornata


F il E did E diFamily Emydidae: Emydinae

1 cross

Clemmys guttata Glyptemys muhlenbergii

1 cross 1 IG

2 spp.


Family Emydidae: Emydinaey y y

Emys blandingiiGlyptemys insculpta 4 crosses 4 IG 4

spp.spp.

Emys orbicularis Actinemys marmorata3rd Small Monobaramin

Wood x Blanding’s Hybridg y

XX

Hybridization in the Emydinae• Emydinae = Clemmys, Glyptemys, Actinemys, Emys

& Terrapenep

GlClemmys guttata

Terrapene spp.

Glyptemys spp.Clemmys guttata

p pp

1 Large Monobaramin?

Emys spp.Actinemys marmorata

Monobaramin?

Emydidae: Deirochelyinae - 1sm.&1l.

Trachemys stejnegeri

2 crosses

T h d T h

3 spp.

Trachemys decorata Trachemys terrapen

1 Small Monobaramin

Family Emydidae: DeirochelyinaeP. concinnaP. floridana

P. alabamensis

P. rubriventris

P. texana

C. picta P. nelsoni

G. psuedogeographica T. scripta

G

G p g g p T p

G hit iG. versa

G hi

G. ouachitensis

G. nigrinodaG. barbouri

G. kohnii

G. oculifera

G. geographica

Hybridization in the Deirochelyinae• Deirochelyinae = Graptemys, Trachemys, Chrysemys,

Psuedemys, Malaclemys & Deirochelys

21 crossesTrachemys scripta Graptemys spp.

21 crosses5 IG

1616 spp.

Chrysemys pictaPseudemys spp.

1 Large Monobaramin

Family Geoemydidae – 2sm.&1l.

Rhinoclemmys punctularia

3

Rhi l l Rhi l di d t

3 crosses 3 spp.

Rhinoclemmys melanosterna Rhinoclemmys diademata


F il G didFamily Geoemydidae1 cross 2 spp.

Mauremys caspica Mauremys rivulata


Family GeoemydidaeM. reevesiiM. japonica

M. mutica

M. annamensis

M. sinensis

M. nigricans Cyc. shanensis

H. grandis S. quadriocellata

R. Pulcherimma(C. America)

S. pseudocellata

C b i i C fl i

G. japonicaMal. subtrijuga

C. trifasciataC. galbinifrons

C. amboinensis

C. mouhotii

C. flavomarginata

C. bourreti

Hybridization in the GeoemydidaeIG26 crosses, 11 IG, 19 species

Geoemyda japonicaHeosemys grandis *Cyclemys shanensis

Cuora spp.Mauremys spp.

Sacalia spp.

1 Large Monobaramin*Large phylogenetic distance Malayemys subtrijugaRhinoclemmys pulcherimma

Proposed Phylogenyf h G d dof the Geoemydidae

*

Spinks et al., 1994*

Discussionl• 288 turtle species

– 41,238 possible hybrids (0.22%)bl f l l h b d ( )– 5,971 possible intra-familial hybrids (1.5%)

• Growing turtle monobaraminsG g– Continue to verify records we already have– Many, as yet, undescribed & undiscovered hybrids M y, y , y

(many in process of being published)– Inclusion of non-hybridizing turtles if they fall within

f f h b d lrange of variation of hybridizing turtles

• We are unable to reject Wood’s (2005) W j W ( 5)hypothesis of five turtle holobaramins

ar i fi t ifi h b idi tia review of interspecific

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