These are the data sumarised in Dulvy, N. K. and J. D. Reynolds. 1997.
Evolutionary transitions among egg-laying, live-bearing and maternal inputs
in sharks and rays. Proceedings of the Royal Society of London. B 264:
1309-1315.
Abstract
Sharks and rays are thought to have a large number of independent origins
of live-bearing. We examined evolutionary transitions to live-bearing and
maternal input in this subclass by optimizing reproductive characters onto
a composite phylogeny. Egg-laying (40% of all species) is the likely
ancestral reproductive mode for this clade, and there is evidence that
live-bearing has evolved independently 9-10 times and maternal input 4-5
times. Most transitions (12-15) have been toward live-bearing with
provisioning limited to yolk. These have occured from egg-laying ancestors
or live-bearing taxa that provide maternal input to embryos. Only 2-3
transitions have occured in the other direction, i. e. away from yolk-only
live-bearing. Egg-laying has evolved from live-bearing ancestors in skates,
Rajidae (25% of all species) and possibly in the zebra shark, Stegostoma
fasciata. Thus, although there has been an overall trend toward the
evolution of live-bearing in elasmobranchs, the evolution of additional
maternal input has been extremely labile.
Name of taxon | Mode of reproduction | CS | References |
---|---|---|---|
Agnatha | Egg-laying, oviparity | 1 | (Cox 1963; Breder and Rosen 1966; Dodd and Dodd 1985) |
Teleostomi | The ancestral state is probably egg-laying | 1 | (Breder and Rosen 1966; Wourms 1981; Wourms 1994; Wourms and Lombardi 1992) |
Placodermi * (7 orders) | Unknown, but there is evidence for internal fertilisation | ? | (Breder and Rosen 1966) |
Rhinochimaeridae (3 genera, 6 spp.) | Egg-laying, single oviparity? | 1 | (Dean 1906) |
Chimeridae (2 genera, 21 spp.) [1] | Egg-laying, single oviparity? | 1 | (Dean 1906; Cox 1963) |
Callorhynchidae (1 genera, 4 spp.) [1] | Egg-laying, single oviparity? | 1 | (Dean 1906; Giacomo 1994) |
Delphyodontus dacriformes * (1 sp.) | Live-bearing; intra-uterine feeding and probably leicithotrophy | 5 | (Lund 1980) |
Myliobatoidei (6 families, 22 genera, 158 spp.) [6] | Live-bearing; leicithotrophic with additional nutrition supplied by histotroph or 'uterine milk'. Trophonemata present | 4 | (Capape 1993; Daiber and Booth 1960; Martin and Cailliet 1988; Snelson, et al. 1988; Wourms 1977; Wourms 1981; Wourms, et al. 1988) |
Rajidae (18 genera, 200+ spp.) [24] | Egg-laying, single oviparity | 1 | (Cox 1963; Fitz and Daiber 1963; Holden 1971; Ishiyama 1958; Richards, et al. 1963) |
Rhinobatoidea (2 families, 9 genera, 51 spp.) [2] | Live-bearing; leicithotrophic with additional nutrition supplied by histotroph or 'uterine milk'. Posesses invaginated uterus walls covered with glandular (possible secretive) cells in R. hynnicephalus. Uterine villi present in R. rhinobatos | 4 | (Bigelow and Schroeder 1953; Abdel-Aziz, et al. 1994; Compagno 1984a; Wenbin and Shuyuan 1993) |
Torpedinoidei (2 families, 11 genera, 38 spp.) [3] | Live-bearing; leicithotrophic with additional nutrition supplied by histotrophe or 'uterine milk'. Uterine villi present | 4 | (Bigelow and Schroeder 1953; Abdel-Aziz 1994; Wourms 1981; Wourms, et al. 1988) Pristiodei |
Pristiodei (1 family, 1 genus, 6 spp.) [1] | Live-bearing; leicithotrophic with additional nutrition supplied by histotroph or 'uterine milk'. Trophonemata present | 4 | (Compagno 1984a; Cook, et al. 1995) |
Pristiophoriformes (2 families, 2 genera, 5spp.) [4] | Yolk-only live-bearing, leicithotrophy or ovoviviparity | 3 | (Compagno 1984a) |
Squatiniformes (1 genus, 12 spp.) [7] | Yolk-only live-bearing, leicithotrophy or ovoviviparity | 3 | (Compagno 1984a; Otake 1990) |
Squaliformes (4 families, 23 genera, 74 spp.) [41] | Yolk-only live-bearing, leicithotrophy or ovoviviparity | 3 | (Breder and Rosen 1966; Wourms 1977; Wourms 1981; Wourms, et al. 1988; Compagno 1984a; Dodd and Dodd 1985; Natanson and Cailliet 1986; Silva 1989; Otake 1990; Vooren 1992) |
Hexanchiformes (4 genera, 5 spp.) [5] | Yolk-only live-bearing, leicithotrophy or ovoviviparity | 3 | (Compagno 1984a) |
Heterodontiformes (1 genus, 8 spp.) [8] | Egg-laying, single oviparity | 1 | (Cox 1963; Compagno 1984a) |
Orectolobiformes (7 families, 14 genera, 31 spp.) [28] | This order exhibits a variety of transistional reproductive forms from oviparity to leicithotrophic live-bearing | . | . |
Hemiscyllium (5 spp.) [5] | Egg-laying, but not confirmed in all spp. | 1 | (Compagno 1984a) |
Pseudoginglymostoma brevicaudatum | Live-bearing; multiple oviparity but egg cases retained, hatching long before partuition | 2 | (Compagno 1984a) |
Ginglymostoma cirratum | Live-bearing; multiple oviparity but egg cases retained, hatching long before partuition | 2 | (Compagno 1984a; Wourms 1977; Wourms, et al. 1988) |
Nebrius ferrugineus | Live-bearing; multiple oviparity but egg cases retained, hatching just before partuition | 2 | (Breder and Rosen 1966; Compagno 1984a; Wourms, et al. 1988) |
Stegastoma fasciata | Egg-laying | 1 | (Breder and Rosen 1966; Compagno 1984a) |
Rhincodon typus | Live-bearing?; delayed multiple oviparity. Previously thought to be oviparous but the jury is still out | 2 | (Baughman 1955; Breder and Rosen 1966; Compagno 1984a; Wourms, et al. 1988; Young, et al. 1996) |
Chiloscyllium (6 spp.) [8] | Egg-laying, but not confirmed in all spp. | 1 | (Smedley 1931; Compagno 1984a) |
Parascyllium (4 spp.) [3] | Egg-laying | 1 | (Compagno 1984a) |
Cirroscyllium ( spp.) [3] | Probably egg-laying | 1 | (Compagno 1984a) |
Brachaelurus waddi | Yolk-only live-bearing; leicithotrophy or ovoviviparity | 3 | (Compagno 1984a) |
Sutorectus tentaculatus | Presumably yolk-only live-bearing; leicithotrophy or ovoviviparity | 3 | [Compagno, 1984a; Dingerkus, 1986] |
Eucrossorhinus dasypogon | Presumably yolk-only live-bearing; leicithotrophy or ovoviviparity | 3 | [Compagno, 1984a; Dingerkus, 1986] |
Orectolobus (4 spp.) [4] | Yolk-only live-bearing; leicithotrophy or ovoviviparity. | 3 | [Compagno, 1984a; Dingerkus, 1986; Otake 1990] |
Lamniformes ( 7 families, 10 genera, 16 spp.) [15] | Live-bearing; nutrition to embryo characterised by either oophagy or adelphophagy (intra-uterine cannibalism). | . | . |
Mitsukurina owstoni | Unknown but presumably vivparous | 5 | (Compagno 1984a; Wourms, et al. 1988) |
Carcharias (=Eugomphodus) (2 spp.) [1] | Live-bearing; leicithotrophy then adelphophagy followed by oophagy . Little known about C. tricuspidatus | 6 | (Compagno 1984a; Gilmore 1993; Springer 1948; Wourms, et al. 1988) |
Odontaspis (2 spp.) [2] | Live-bearing, leicithotrophy followed by oophagy | 5 | (Compagno 1984) |
Pseudocarcharias kamoharai | Live-bearing, leicithotrophy followed by oophagy | 5 | (Compagno 1984; Gilmore 1993) |
Megachasma pelagios | Live-bearing, leicithotrophy followed by oophagy | 5 | (Castro, et al. 1996; Compagno 1984a) |
Alopius (3 spp.) [2] | Live-bearing, leicithotrophy followed by oophagy, Gilmore suggests that these spp. may be capable of adelphophagy but there is no direct evidence | 5 | (Compagno 1984a; Wourms, et al. 1988; Otake 1990; Gilmore 1993) |
Cetorhinus maximus | Live-bearing, leicithotrophy followed by oophagy | 5 | (Compagno 1984a; Gilmore 1993; Wourms 1977; Wourms, et al. 1988) |
Lamna (2 spp.) [2] | Live-bearing, leicithotrophy followed by oophagy; adelphophagy unlikely | 5 | (Wourms 1977; Wourms, et al. 1988; Compagno 1984a; Otake 1990; Gilmore 1993) |
Carcharodon carcharias | Live-bearing, leicithotrophy followed by oophagy; adelphophagy unlikely | 5 | (Compagno 1984a; Francis 1996; Gilmore 1993; Wourms, et al. 1988) |
Isurus (2 spp.) [2] | Live-bearing, leicithotrophy followed by oophagy; adelphophagy unlikely | 5 | (Compagno 1984a; Gilmore 1993; Wourms, et al. 1988) |
Carcharhiniformes (7 families, 47 genera, 208 spp.) [148] | . | . | . |
Apristurus (25 spp.) [10] | Single oviparity | 1 | (Cox 1963; Breder and Rosen 1966; Compagno 1984b; Compagno 1988; Nakaya 1975; Wourms, et al. 1988) |
Cephalurus cephalus | Live-bearing; single oviparity but eggs are retained until hatch | 1 | (Compagno 1984b; Compagno 1988) |
Parmaturus (4 spp.) [1] | Single oviparity | 1 | (Cox 1963; Compagno 1984b; Compagno 1988) |
Galeus (10 spp.) [7] [1] | Single oviparity | 1 | (Compagno 1984b; Compagno 1988; Nakaya 1975; Wourms 1981) |
G. polli | Yolk-only live-bearing; eggs retained until hatch | 1 | (Compagno 1984b; Compagno 1988) |
G. arae | Multiple oviparity | 2 | see refs above |
G. melastomus | Multiple oviparity | 2 | see refs above |
Asymbolus (2 spp.) [2] | Egg-laying, single oviparity | 1 | (Compagno 1984b; Compagno 1988) |
Halaelurus 11 spp. in total) [4] | . | . | (Compagno 1984b; Compagno 1988; Nakaya 1975; Wourms, et al. 1988) |
H. boesemani | Multiple oviparity with egg retention | 2 | Compagno 1984b |
H. buergeri | Multiple oviparity, egg capsules retained until an advanced stage of development is reached whereupon they are laid | 2 | Nakaya 1975; Compagno 1984b |
Halaelurus subgenus Bythaelurus (6spp.) [1] | Single and multiple oviparity | 1,2 | See refs above |
Haploblepharus (3 spp.) [3] | Egg-laying, single oviparity | 1 | (Breder and Rosen 1966; Compagno 1984b; Compagno 1988) |
Holohalaelurus (2 spp.) [2] | Egg-laying, single oviparity | 1 | ( Compagno 1984b; Compagno 1988) |
Schroederichthyinae (4 spp.) [3] | Egg-laying, single oviparity | 1 | (Compagno 1984b; Compagno 1988; Gomes & de Carvalho 1995) |
Scyliorhinus (13 spp.) [11] | Egg-laying, single oviparity | 1 | (Compagno 1984b; Compagno 1988; Nakaya 1975; Wourms, et al. 1988; Gomes & de Carvalho 1995) |
Cephaloscyllium (7 spp.) [5] | Egg-laying, single oviparity | 1 | (Cox 1963; Nakaya 1975; Compagno 1984b; Compagno 1988; Otake 1990) |
Poroderma (3 spp.) [2] | Egg-laying, single oviparity | 1 | (Compagno 1984b; Compagno 1988) |
Atelomycterini (2 genera, 2 spp) [3] | Egg-laying, single oviparity | 1 | (Breder and Rosen 1966; Compagno 1984; Compagno 1988) |
Proscyllium habereri | Egg-laying, single oviparity | 1 | (Compagno 1984; Compagno 1988; Wourms, et al. 1988) |
Ctenacis fehlmanni | Egg-laying, possibly retained for some time before laying | 1 (2?) | (Compagno 1984; Compagno 1988) |
Eridacnis (3 spp.) [3] | . | . | (Compagno 1984b; Compagno 1988) |
E. barbouri | Yolk-only live-bearing, leicithotrophy or ovoviviparity | 3 | See refs above |
E. radcliffi | Yolk-only live-bearing, leicithotrophy or ovoviviparity | 3 | See refs above |
E. sinuans | Yolk-only live-bearing, leicithotrophy or ovoviviparity | 3 | See refs above |
Gollum attenuatus | Live-bearing; matrotrophic, oophagy & uterine milk. Feeds on yolk of broken down eggs within egg sac | 5 | (Compagno 1984; Compagno 1988; Yano 1993) |
Pseudotriakis microdon | Live-bearing; matrotrophic, oophagy & uterine milk | 5 | (Compagno 1984b; Compagno 1988; Yano 1992) |
Leptocharias smithii | Live-bearing; matrotrophy via globular or spherical placenta | 7 | (Compagno 1984b; Compagno 1988; Wourms, et al. 1988) |
Triakis (5 spp.) [5] | Yolk-only live-bearing, leicithotrophy or ovoviviparity | 3 | (Compagno 1984b; Compagno 1988; Otake 1990) |
Scylliogaleus quecketti | Yolk-only live-bearing, leicithotrophy or ovoviviparity | 3 | (Compagno 1984b; Compagno 1988) |
Mustelus (20 spp.) [20] | Yolk-only live-bearing, leicithotrophy or ovoviviparity | 3 | (Nakaya 1975; Teshima 1975; Teshima 1981; Wourms 1977; Wourms, et al. 1988; Compagno 1984b; Compagno 1988; Dodd and Dodd 1985; Otake 1990; Vooren 1992) |
M. antarticus | Live-bearing; matrotrophy, placenta & uterine villi | 8 | See refs. above |
M. canis | Live-bearing; matrotrophy, placental & uterine milk | 8 | See refs. above |
M. mustelus | Live-bearing; matrotrophy, placental nutrition | 8 | See refs. above |
M. fasciatus | ? | 7 | See refs. above |
M. griseus | Live-bearing; matrotrophy, highly active secretive intra-uterine epithelium & placenta. Egg membrane incorporated into placenta | 7 | (Teshima 1975; Teshima 1981; Otake 1990) |
M. henlei | ? | 7 | See refs. above |
Golgolia filewoodi | Yolk-only live-bearing, leicithotrophy or ovoviviparity | 3 | (Compagno 1984b; Compagno 1988; Vooren 1992) |
Hemitriakis (2 spp.) [2] | Yolk-only live-bearing, leicithotrophy or ovoviviparity | 3 | (Compagno 1984b; Compagno 1988) |
Iago (2 spp.) [2] | Live-bearing; matrotrophic, placenta | 7 | (Compagno 1984b; Compagno 1988) |
Furgaleus macki | Yolk-only live-bearing, leicithotrophy or ovoviviparity | 3 | (Compagno 1984b; Compagno 1988) |
Paragaleus (3 spp.) [3] | Live-bearing; matrotrophic, placenta & appendiculae | 8 | (Compagno 1984b; Compagno 1988) |
Hemigaleus microstoma | Live-bearing; matrotrophic, placenta & appendiculae | 8 | (Compagno 1984b; Compagno 1988) |
Chaenogaleus macrostoma | Live-bearing; matrotrophic, placenta | 7 | (Compagno 1984b; Compagno 1988) |
Hemipristis elongatus | Live-bearing; matrotrophic, placenta & appendiculae | 8 | (Compagno 1984b; Compagno 1988) |
Hypogaleus hyugaensis | Live-bearing, placenta | 7 | (Compagno 1984b) |
Galeorhinus galeus | Yolk-only live-bearing, leicithotrophy or ovoviviparity | 3 | (Compagno 1984b; Vooren 1992) |
Galeocerdo cuvier | Yolk-only live-bearing, placenta possibly lost. This species is thought to be matrotrophic but the mechanism of nutrient transfer is unknown | 3 | (Compagno 1984b; Compagno 1988; Wourms, J. P. pers. comm.) |
Scoliodon laticaudus | Live-bearing; matrotrophic, placenta (trophonematal cup) & appendiculae. Uterine epithelium has high secretory activity | 8 | (Compagno 1988; Wourms, et al. 1988; Wourms 1993; Otake 1990) |
Eusphyrna blochii | Live-bearing; matrotrophic, placenta & appendiculae | 8 | (Compagno 1984b; Stevens and Lyle 1989) |
Sphyrnidae (8 spp.) [7] | Live-bearing; matrotrophic, placenta & appendiculae | 8 | (Schlernitzauer and Gilbert ????; Compagno 1984b; Compagno 1988; Dodd and Dodd 1985; Hamlett 1986; Stevens and Lyle 1989) |
Rhiziprionodon (7 spp.) [6] | Live-bearing; matrotrophic, placenta & appendiculae | 8 | (Compagno 1984b; Compagno 1988; Hamlett 1986; Wourms 1977) |
Loxodon macrorhinus | Live-bearing; matrotrophic, placenta & appendiculae | 8 | (Compagno 1984b; Compagno 1988) |
Isogomodon oxyrhynchus | Live-bearing; matrotrophic, placenta | 7 | (Compagno 1984b; Compagno 1988) |
Trianodon obesus | Live-bearing; matrotrophic, placenta | 7 | (Compagno 1984b; Compagno 1988) |
Carcharhinus porosus group (8 spp.) [6] | Live-bearing; matrotrophic, placenta | 7 | (Compagno 1984b; Compagno 1988) |
Carcharhinus acronotus group (6 spp.) [6] | Live-bearing; matrotrophic, placenta | 7 | (Compagno 1984b; Compagno 1988) |
Nasolamia velox | Live-bearing; matrotrophic, placenta | 7 | (Compagno 1984b; Compagno 1988) |
Carcharhinus obscurus group (6 spp.) [5] | Live-bearing; matrotrophic, placenta | 7 | (Compagno 1984b; Compagno 1988) |
Carcharhinus ambionensis group (2 spp.) [1] | Live-bearing; matrotrophic, placenta | 7 | (Compagno 1984b; Compagno 1988) |
Negaprion (2 spp.) [2] | Live-bearing; matrotrophic, placenta | 7 | (Compagno 1984b; Compagno 1988) |
Lamniopsis temmincki | Live-bearing; matrotrophic, placenta | 7 | (Compagno 1984b; Compagno 1988) |
Glyphis (2 spp.) [1] | Live-bearing; matrotrophic, placenta | 7 | (Compagno 1984b; Compagno 1988) |
Prionace glauca | Live-bearing; matrotrophic, placenta & trophonemata. Intra-uterine epithelium is non-secretory, but may be important for uterine fluid osmoregulation | 8 | (Compagno 1984b; Compagno 1988; Wourms, et al. 1988; Otake 1990) |
Carcharhinus brevipinna group (5 spp.) [3] | Live-bearing; matrotrophic, placenta | 7 | (Compagno 1984b; Compagno 1988) |
Carcharhinus perezi group (3 spp.) [2] | Live-bearing; matrotrophic, placenta | 7 | (Compagno 1984b; Compagno 1988) |
Created February 1998; revised Februray 1998.