Evolution of Viviparity in Salamanders (Amphibia, Caudata)

Abstract

Reproductive modes in salamanders (Amphibia, Caudata) are highly diverse. Viviparity, for instance, implies the retention of the developing embryos inside the females until the end of the gestation, at which point they deliver fully developed terrestrial juveniles. From an ecological point of view, the evolution of viviparity is highly significant, since it implies the semi‐independence of water for an amphibian. Nevertheless, viviparity is not very common among salamander. It has independently evolved only in a few species, all included within the family Salamandridae. Furthermore, the characteristics of viviparous strategies are different among species, although they all share some commonalities. The detailed study of these particular and common features in a phylogenetic context will reveal the genetic, physiological, developmental, morphological and historic factors that have triggered the evolution of this peculiar mode of reproduction in only one lineage among all the species of salamanders. Key Concepts: Viviparity entails the complete development of the progeny within the mother's genital tract, together with the maternal provisioning of nutrients to the embryos. Since development occurs within the females, viviparity in amphibians implies that the aquatic phase of the standard amphibian life cycle is obviated in viviparous species. Viviparity has independently evolved only in a few species of salamanders.

Evolution of vertebrate viviparity and specializations for fetal nutrition: A quantitative and qualitative analysis

“… Estimates of the percentage of extant species that are viviparous are based on the following sources: Blackburn, ; Buckley, ; Wourms and Lombardi, . One recent source estimates the percentage of viviparous species in elasmobranchs to be 40% (Dulvy and Reynolds, ).…”

“…In urodeles, viviparity is rare. However, European salamandrids of two genera ( Salamandra and Lyciasalamandra ) are viviparous; parsimoniously they stem from a single common origin of this pattern (Buckley, ). The widely distributed populations differ in terms of whether females give birth to larvae (“larviparity”; Greven, ) or to metamorphosed offspring (pueriparity); in the latter case, embryos are supplied with nutrients via matrotrophy (see below).…”

“… Literature sources: 1) Blackburn, ; 2) Blackburn, ; 3) Blackburn, ; 4) Blackburn, ; 5) Blackburn and Callard, ; 6) Blackburn and Flemming, ; 7) Blackburn and Flemming, ; 8) Blackburn and Flemming, ; 9) Blackburn and Vitt, ; 10) Blackburn and Vitt, 2002; 11) Buckley, ; 12) Buckley et al, ; 13) Exbrayat and Hraoui‐Bloquet, ; 14) Flemming and Branch, ; 15) Ghiara et al, ; 16) Gower et al, ; 17) Greven, ; 18) Jerez and Ramírez‐Pinilla, ; 19) Ramirez, 2006; 20) Ramírez‐Pinilla et al, ; 21) Ramirez‐Pinalla et al, 2011; 22) Shine, ; 23) Stewart and Thompson, ; 24) Stewart and Thompson, ; 25) Stewart and Thompson, ; 26) Thompson et al, ; 27) Thompson et al, ; 28) Xavier, ; 29) Xavier, ; 30) Wake, ; 31) Wake, ; 32) Wake, ; 33) Wake, ; 34) Wake, ; 35) Wake, ; 36) Wake and Dickie, .…”

A review of the reproductive biology of the only known matrotrophic viviparous anuran, the West African Nimba toad, Nimbaphrynoides occidentalis

“…As most caudates (90%, Wake 2015a) and all caecilians are internally fertilising (Gomes et al 2012, Wake 2015a) they show the first requirement for viviparity (Wake 2015a(Wake , 2015b. Nineteen (2.7%, Buckley 2012) of the ca 700 caudate species (695 AmphibiaWeb 2017, 703 Frost 2017, both accesses 11.01.2017) and about one fourth of the ca 200 caecilian species (205 AmphibiaWeb 2017, 205 Frost 2017, both accessed 11.01.2017) are known or assumed to be viviparous (Buckley 2012, San Mauro et al 2014, Wake 2015a, 2015b. Anurans (frogs and toads), on the other hand, show a very high diversity in reproductive modes (at least 42 modes, Haddad andPrado 2005, Iskandar et al 2014), but internal fertilisation and viviparity are very rare.…”

“…The best-known example for matrotrophy are mammals, in which yolk poor eggs are fertilised and very early within the development the nutritional needs of the foetus are provided for by the mother via a placenta. Nutrition through unfertilised eggs and/ or intra-oviductal cannibalism of the offspring, is known for example from Salamandra salamandra subspecies (Buckley et al 2007, Buckley 2012. Matrotrophy in amphibians may be achieved through the development of a particular intra-oviductal epithelium (e.g.…”