* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Download Oviparity or viviparity? That is the question…
Survey
Document related concepts
Cheating (biology) wikipedia , lookup
History of biology wikipedia , lookup
Developmental biology wikipedia , lookup
Introduction to evolution wikipedia , lookup
Saltation (biology) wikipedia , lookup
Evolution of sexual reproduction wikipedia , lookup
Maternal effect wikipedia , lookup
Evolutionary history of life wikipedia , lookup
Inclusive fitness wikipedia , lookup
Koinophilia wikipedia , lookup
Transcript
reproductive biology 12 (2012) 259–264 Available online at www.sciencedirect.com journal homepage: http://www.elsevier.com/locate/repbio Review Article Oviparity or viviparity? That is the question. . . Thierry Lodé UMR-CNRS 6552 Ethos, University of Rennes 1, 35042 Rennes cedex, France article info abstract Article history: The modes of reproduction undoubtedly represent one of the most critical life-history traits Received 7 November 2011 because they profoundly affect fitness and survival. The parent–offspring conflict over the Accepted 5 April 2012 degree of parental investment may be the main selective factor in the evolution of reproduction. Although the modes of sexual reproduction are remarkably diversified in animals, Keywords: the traditional typology spanning three classes does not seem to be adequate to clarify the Egg retention level of parental investment. Thus, lecithotrophy does not provide any information on the Fertilization retention of the zygotes inside the parent’s body and matrotrophy only indicates that Oviparity nutrients are provided by mother but does not make any distinction between various types Ovuliparity of maternal care. I here present a scientific typology of the reproductive modes comprising five Lecithotrophy classes: ovuliparity, oviparity, ovo-viviparity, histotrophic viviparity and hemotrophic viviparity. Matrotrophy Based on the development stage of the zygote and on its interrelation with the parent, my Placenta classification details the degree of contrivances by which animals provide alternative parental Reproduction investment in their offspring. Hence, this typology possesses a great heuristic value, both in Viviparity reproduction and evolutionary biology. These different modes of reproduction do represent a sequence, with ovuliparity being the most primitive and hemotrophic viviparity the most Zygote advanced mode. Lastly, the comparative analysis of different reproductive modes in vertebrates suggests that climatic conditions (cold) could be one of the strongest selection pressures for extending egg retention and the establishment of viviparity. # 2012 Society for Biology of Reproduction & the Institute of Animal Reproduction and Food Research of Polish Academy of Sciences in Olsztyn. Published by Elsevier Urban & Partner Sp. z o.o. All rights reserved. 1. Introduction Animals have evolved, in a range of reproductive adaptations, from oviparity to viviparity. The natural evolution of these two different modes of sexual reproduction brought about an increase in parental investment during phylogeny [1,2]. Numerous animal species devote considerable energy to protecting their eggs and to raising and feeding their offspring, and some can even take care of their own zygotes before birth, enhancing the offspring’s chance to survive. Parental care in turn influences mating strategies and the Trivers’ model argues that individuals with higher level of parental investment become increasingly selective in their choices of a mate(s). It may be deduced that parental care promoted the evolution of the more complex modes of reproduction. Although in some species with external fertilization males show a greater degree of parental care, females generally invest more in offspring than males [3]. Provided additional E-mail address: [email protected] (T. Lodé). 1642-431X/$ – see front matter # 2012 Society for Biology of Reproduction & the Institute of Animal Reproduction and Food Research of Polish Academy of Sciences in Olsztyn. Published by Elsevier Urban & Partner Sp. z o.o. All rights reserved. http://dx.doi.org/10.1016/j.repbio.2012.09.001 260 reproductive biology 12 (2012) 259–264 nutrition to offspring should be favored by natural selection due to the consequent increase in the offspring’s fitness [4,5], but retaining the zygotes and early embryos within the female’s body is a strategy whereby numerous animals protect their offspring during the most vulnerable stage of their development. It has been proposed that the parent–offspring conflict over the degree of parental investment is one of the main determining factors in the evolution of reproductive strategies [6]. The reproductive modes certainly influence the level at which males reduce or increase their parental care, and alternative forms of embryo nutrition allow parents to ‘‘redirect’’ their parental investment. In general, all birds and prototherian mammals are oviparous, while therian mammals are viviparous, but the modes of reproduction are remarkably diversified, especially in arthropods, fish-, reptiles and amphibians. Some of the latter groups have even developed certain aspects of viviparous development. For instance, the fire salamander is considered to exhibit an ovo-viviparous reproductive mode, but some subspecies such as Salamandra s. fastuosa or Salamandra s. bernadezi show viviparous development with the fully metamorphosed offspring [7,8]. Likewise, the black salamander Salamandra atra gives birth to live young [9]. The viviparity of salamanders could be an adaptation to the shortage of water, caused by either the harsh mountain climate or droughts [9,10]. Therefore, these reproductive modes are not only the consequence of the phylogeny but also the adaptive responses to environmental constraints. For example, the common lizard Lacerta/Zootoca vivipara lays eggs in mountains but exhibits an ovo-viviparous development in plains [11–14]. Such variations in reproductive strategies and the different modes of fertilization and retention of the fertilized eggs within the maternal body lead to a certain confusion when it comes to the use of terms ‘‘oviparity’’ and ‘‘viviparity’’. Oviparity is assumed to be the ancestral condition in lineages of animals but the term encompasses a broad range of situations. Oviparity is generally defined as ‘‘any spawning of oocytes (unfertilized) or fertilized eggs’’ and viviparity is defined as ‘‘any mechanism for live-bearing or maintenance of development, by either maternal or paternal parent in or on any part of the body’’, while ovoviviparity straddles both modes [15]. In fact, this classification of different modes of reproduction into three classes is rather old-dated and is primarily based on empirical observations; therefore, so much confusion is still associated with this descriptive classification especially in light of the well-known variety of reproductive strategies [16]. Thus, if birds are classified as oviparous, could numerous fish, such as salmonids, be considered oviparous as well since the females do not spawn eggs but produce only unfertilized ova? The use of the term ‘‘ovuliparity’’ appears to be most adequate when fertilization is external [17]. Similarly, many fish are considered viviparous without showing the typical mammalian reproductive characteristics such as placentation [18]. And what about the classification of the species regarded as ovo-viviparous or viviparous but whose embryonic development does not occur inside the genital tract of the female but rather in the organs such as the vocal sacs of the male toad Rhinoderma [19] or the ventral pouch of the male seahorse? Both the oviparity and viviparity are traditionally defined on the basis of the final developmental stage of the offspring, but such definitions, which are lacking the inclusion of the preceding species-related adaptations, simply remain insufficient to fully describe the reproductive modes [16,20]. The variety of previously mentioned reproductive strategies implies that the parental investment and the parent–offspring conflict could also extend onto all processes that occur inside the bodies of the adults, especially the female. It has been proposed that the classification of reproductive modes should take into account the source of nutrients for embryonic development, distinguishing the nutrients derived from the yolk (i.e. lecithotrophy) from those provided by the mother (i.e. matrotrophy [21]). At present, matrotrophy is regarded as the feeding of the zygote by the mother and there is no distinction between the specific evolutionary types of this mode of nutrition, histotrophy and hemotrophy, whereas the two distinct types of nutritional viviparity should be clearly distinguished, emphasizing the level of parental investment associated with them. Similarly, the term lecithotrophy does not provide any information on the retention of zygotes inside the body as it is based only on the ‘‘old’’ definitions of oviparity and viviparity [22]. Finally, numerous classes of animals include both oviparous and viviparous species, which should provide a basis for a new classification of the evolution of reproduction [5]. 2. A new typology of reproductive modes – a proposal The objective of the proposed classification is not to detail all anatomical and physiological features of different modes of sexual reproduction, but to provide a scientific typology compatible with some characteristic examples. Based on the relationships between the parents and offspring, including a typology of fertilization and early embryonic development (i.e. external fertilization, internal fertilization, retention of eggs or embryos, stages of embryonic development) and the mode of nutrient intake (i.e. feeding external oophagy, intrauterine cannibalism, histotrophic or hemotrophic supply), I propose the following five categories of different reproductive modes: ovuliparity, oviparity, ovo-viviparity, histotrophic viviparity and hemotrophic viviparity. As it acknowledges the relationships between parental investment and embryonic development, such a classification appears to be highly relevant in the context of evolutionary biology (Table 1). 2.1. Ovuliparity Ovuliparity refers to the release of oocytes from the female reproductive tract. Therefore, a species is considered ovuliparous when the female emits ova in the environment and the ova are then fertilized externally by the male. Ovuliparity is hence characterized by the external fertilization; the male sprays milt on the ova, which can sometimes be deposited in a nest. The chorion develops from the surface of the yolk sac. The fertilized eggs continue their development in the environment outside the body of the parents. In many mollusks, arthropods and fish, females lay ova on the breeding sites where the male will carry out fertilization. These sites include hollows in gravels as with trout Salmo trutta or even the 261 reproductive biology 12 (2012) 259–264 Table 1 – Typology of the reproductive modes (five classes) with the description of a degree of parental investment. Reproductive mode Variety Ovuliparity Oviparity Ovo-viviparity Histotrophic viviparity Hemotrophic viviparity Single oviparity Multiple oviparity (retention before spawning) Organic retention (deriving from parental care) Oviductal retention Adenotrophy Skin feeding Oophagy Adelphophagy Pseudo-placenta Real placenta: - Omphaloplacenta - Allantoplacenta Retention/protection External fertilization, no retention of eggs Protected internal fertilization, no or limited retention Moderate quantity of nutriments in the ova ‘‘Lecithotrophy’’ High quantity of yolk Clutch retention until hatching and incubation in a parent body ‘‘Lecithotrophy’’ Only moderate quantity of yolk, no additional supply ‘‘Matrotrophy’’ Low quantity of yolk, but additional supply by feeding on organic tissues (glandular or skin feeding, oophagy or adelphophagy) ‘‘Matrotrophy’’ Very low quantity of yolk, but additional nutriments provided through mother’s bloodstream (pseudo or real placenta) Young development in the female body Young development in the female body building of quite a complex nest, as with the stickleback Gasterosteus aculeatus. Generally, the larvae hatch after a brief period of embryonic development. In the Eleutherodactylidae family, the froglets hatch directly from the eggs with no tadpole stage [23]. Ovuliparity is a primitive mode of reproduction. Typically, toads and frogs amplexus [24] are the examples of ovuliparity. 2.2. Supply Oviparity Oviparity is characteristic of species with the internal fertilization with the embryos being set up in the genital tract of the female. Oviparity is typically the lecithotrophic reproduction, where the eggs are provided with an abundant yolk. The egg is generally associated with a chorion and is often protected by a robust, complex and durable eggshell [25,26]. After spawning, the embryonic development will continue outside the body of the female, without any direct nutritive interaction. However, parents may develop specific interactions with the brood (e.g. incubation). Oviparity could be single (each egg laid individually) or multiple (some eggs are briefly retained and then spawned together with the more recent ones). Typically, birds show external oviparous reproduction, laying an egg provisioned with an abundant yolk. However, no feature of avian reproduction is known to be incompatible with the viviparous reproduction [27]. The reason why all birds exhibit oviparous reproduction could be the fact that as warm-blooded animals they can externally incubate their eggs, something that amphibians and reptiles cannot do. In oviparous animals, most poikilotherms use nests to retain heat to incubate eggs, but this requires optimal, warm environmental conditions. This also suggests that ambient temperature could have been one of the strongest selection pressures for egg retention and viviparity. Viviparity evolved in cold climate reptiles only when the females were able to maintain stable body temperature [28]. Skate (rajiforms) and scyliorhinids show multiple oviparity; several egg cases can accumulate in each oviduct before spawning [20,29]. The multiple oviparity appears to be an intermediate stage between the single oviparity and the reproductive mode characterized by an extended retention of eggs (i.e. ovo-viviparity). The primitive prototherian mammals such as the platypus or echidnas are oviparous. 2.3. Ovo-viviparity Ovo-viviparity is characterized by an internal incubation, or a prolonged retention of fertilized eggs during the embryonic development, but with no direct nutritive exchange between the parent and the embryo. Fertilization can be external or internal but the embryonic development will continue inside the parent’s body so that ovo-viviparity is often the lecithotrophic reproduction. Several different mechanisms of ‘‘embryo retention’’ have evolved in fish, amphibians and reptiles. Retention of fertilized eggs occurs most often in the oviduct, but the internal fertilization is required for oviductal retention of the embryo. When other organs are used for incubation of the eggs, the externally fertilized zygotes are ingested or deposited in these organs. Nevertheless, the organic retention (i.e. skin brooding, mouth or stomach incubation) probably derives from the parental care of juveniles, whereas the oviductal incubation could be a first stage in the development of viviparity retention, as suggested by the thinness of the shell. The thinning of the shell evolves in parallel to the increase in egg retention. For instance, in numerous ovo-viviparous species such as the lizard Scleropus scalaris, after a period of internal incubation, the very thin eggshell is destroyed when the female expels the young [30]. It seems that retention of developing eggs in the uterus by oviparous squamates enhances maternal fitness due to accelerated developmental rates of eggs in utero as compared to in the nest [31]. 2.4. Histotrophic viviparity This mode of reproduction is characterized by the development of embryos inside the female’s body and with a steady supply of nutrients. Fertilization is hence internal but in addition to the yolk, the maternal nutrition is provided (‘‘matrotrophy’’). The term aplacental viviparity that was 262 reproductive biology 12 (2012) 259–264 formerly used should be abandoned as it refers to the ‘‘absence’’ of a placenta and is uninformative. Similarly, the term ‘‘matrotrophy’’ only refers to maternal feeding, with no information on the characteristics of nutrition. Nutrient input into the oviduct during embryonic development results in a small number of offspring, usually one per oviduct. Glandular secretion (i.e. adenotrophy) may contribute to the offspring’s nutrition. As suggested by the occurrence of viviparity in amphibians, reptiles and mammals, the viviparity may have evolved as an evolutionary response to cold climatic conditions in animals that were able to keep their body temperature stable. Many insects show adenotrophic viviparity (i.e. when offspring are supplied by specialized glandular secretions) such as in diptera (glossinidae flies, mosquitoes) or lepidoptera (moths). Eggs, with a chorion, are retained within the female’s body and are nourished through glandular secretion until the developed larvae are ready to pupate. It should be noted that the extended retention of eggs in the oviducts evolved concurrently with a reduction in egg yolk content; this process influenced by progesterone led to the formation of vascular connections between the mother and the embryo, and the development of placenta-like structures in hemotrophic viviparity. The oviductal gestation occurs in some caecilian amphibians whose males possess an intromission organ, the phallodeum (i.e. with internal fertilization). Larvae are equipped with a form of dentition that they use to eat the outer layer of their mother’s modified skin [32]. The female can also feed the offspring through the production of ova that are consumed by the young (i.e. oophagy). In some cases, the first embryo to hatch inside the female’s body can feed on other eggs and even directly on other larvae; this is referred to as the intra-uterine cannibalism or adelphophagy. For example, the black salamander S. atra produces only two offspring (one per oviduct) that attain full development through the intra-uterine cannibalism [9]. It is generally assumed that this adaptation promotes survival of these species, which are exposed to cold and shortage of water. Histotrophic viviparity also exists in elasmobranchs such as Carcharias taurus or shortfin mako Isurus oxyrinchus in which embryos feed on eggs and other embryos (oophagy and adelphophagy [33,34]). Numerous lamniforms continuously produce unfertilized eggs on which the developing embryos feed [26,35]. 2.5. Hemotrophic viviparity Fertilization and embryogenesis occur in the female genital tract. The growing embryo draws the continuous nourishment from the mother (matrotrophy), usually through a placenta or a similar structure (i.e. hemotrophy). Associated with the production of a yolkless egg, the hemotrophic viviparity is a mode of reproduction in which embryonic development is exclusively stimulated by nutrient inputs from the bloodstream of the parent. The bloodstreams of the mother and the embryo are separated by a physical barrier, but a placenta or placentalike structures enable the exchange of nutrients and waste products [36]. Viviparity involves the direct contact of maternal and embryonic tissues, with a shared surface facilitating respiratory and metabolic exchange. The embryonic development often occurs in a specialized organ, such as the uterus, and the zygote can be implanted at various depths within the mucosa. In the frogs Nectophrynoides occidentalis, Gastrotheca marsupiata and Gastrotheca ovifera, the gills of tadpoles have foliaceous expansions, which allows for the transport of nutritive fluid from the maternal, richly vascularized tissues [37–41]. We can therefore classify these frogs as viviparous since the nutrient intake appears through the bloodstream of the parent. The caecilian Typhlonectes larvae also show highly vascular gill structures that probably function as a pseudoplacenta [42]. Uterine specializations are also found in elasmobranchs Rhizoprionodon terraenovae and Carcharhinus plumbeus, in which the uterus assumes the function of providing nutrients to the developing embryos after the yolk stores have been depleted. This structure is able to transfer nutriments from the maternal vascular system [35]. Some teleosts are known to develop a pseudo-placenta enabling viviparity, but because there is no attachment between embryonic and maternal tissues, the maternal–embryonic exchange is mediated by the uterine wall [43,44]. The ovarian wall becomes hyper-vascularized and embryotrophic proteins can be absorbed from the maternal serum [45]. In some skink lizards, the embryo can absorb nutriments through extraembryonic vascular annexes [11,13,15]. In mammals, the developing fetuses are connected to a special membranous organ with a rich blood supply, the placenta that lines the uterus in pregnant females and provides nourishment to the fetus. In metatherian mammals, an omphaloplacenta reinforces the embryo–mother interactions, but in therian mammals, the allantoplacenta, formed by both the uterine mucosa and fetal membranes, governs the exchange of nutrients and waste products. 3. Discussion It is possible to eliminate the confusion associated with the use of traditional terms describing the modes of sexual reproduction by applying the new and rigorous scientific typology proposed in this review article. Each of the five proposed categories is clearly defined, without ambiguity in classifying the species whose reproductive habits are well known. Furthermore, such a typology of sexual reproductive modes emphasizes the role of parental investment and relationships between the parents and their offspring, illustrating the evolutionary transitions from ovuliparity and oviparity to viviparity [46]. Sexual reproduction evolved as the privileged mode of reproduction in eukaryotes and the genetic exchange generally appears to be a very archaic process, occurring in primitive steps of proto-cell development [46–48]. The proposed modes of reproduction do represent a sequence in a continuum with ovuliparity as the most primitive and hemotrophic viviparity the most advanced mode. Egg/embryo retention and then histotrophy appear to be logical steps in the evolution of viviparity, and they are achieved through a decline in ovum size, reduction of eggshells, maternal nutrition and modification of uterine tissues, and further changes in embryo morphology. The evolutionary shift between oviparity and viviparity presumably occurs via increased duration of egg retention and an reproductive biology 12 (2012) 259–264 increase in vascularity of embryonic and maternal tissues [49,50]. Thus, skin feeding, oophagy, adelphophagy and adenophagy may constitute the primitive and intermediate stages for the fetal feeding inside the oviduct of viviparous animals, while the initial growth of oviparous animals chiefly depends on the provision of yolk. In fact, providing an embryo with nutrition inside the parent’s body should be promoted by natural selection as it is associated with the increased fitness of the offspring but reduced fecundity [15]. Likewise, the consequences for offspring fitness of the duration of egg retention may result in a trade-off in ovo-viviparity modes. Although any evolutionary change requires trade-offs, the life-history traits such as the modes of reproduction are undoubtedly the most critical evolutionary features because they affect fitness and survival so profoundly [5,51]. The adaptive significance of the inter-species variations suggests that selective pressures, and especially environmental conditions (cold), may favor anatomical and physiological adaptations of the mother and embryos for viviparity. As the proposed typology of the reproductive modes is based on the features of embryonic development, the existence and duration of egg/embryo retention and the mode of nutrient intake, it appears to have a great heuristic value in both the reproductive and evolutionary biology. references [1] Clutton-Brock TH. The evolution of parental care. Princeton, USA: Princeton University Press; 1991. [2] Trivers RL. In: Campbell B, editor. Sexual selection and the descent of man 1871–1971. Chicago, USA: Aldine-Atherton; 1972. p. 136–79. [3] Andersson M. Sexual selection. Princeton, USA: Princeton University Press; 1994. [4] Reynolds JD, Goodwin NB, Freckleton RP. Evolutionary transitions in parental care and live bearing in vertebrates. Philosophical Transactions Royal Society London B 2002; 357:269–81. [5] Shine R. Reconstructing the adaptionist scenario: what selective forces favor the evolution of viviparity in montane reptiles? American Naturalist 2002;160:582–93. [6] Crespi BJ, Semeniuk C. Parent-offspring conflict in the evolution of vertebrate reproductive mode. American Naturalist 2004;163:635–53. [7] Dopazo H, Alberch P. Preliminary results on optional viviparity and intrauterine siblicide in salamandra salamandra populations from Northern Spain. Mertensiella 1994;4:125–37. [8] Joly J, Chesnel F, Boujard D. Biological adaptations and reproductive strategies in the genus Salamandra. Mertensiella 1994;4:255–69. [9] Vilter V, Vilter A. On pregnancy of the black Salamander Salamandra atra Laur (in French). Comptes Rendus Société Biologique 1960;154:290–4. [10] Buckley D, Alcobendas M, Garcia-Paris M, Wake MH. Heterochrony, cannibalism, and the evolution of viviparity in Salamandra salamandra. Evolution & Development 2007;9:105–15. [11] Guillette Jr LJ. The evolution of viviparity in lizards. BioScience 1993;43:742–51. [12] Panigel M. Contribution to the study of ovoviviparity in reptils: gestation and parturition of viviparous lizard [13] [14] [15] [16] [17] [18] [19] [20] [21] [22] [23] [24] [25] [26] [27] [28] [29] [30] [31] [32] [33] [34] [35] 263 Zootoca vivipara (in French). Annales des Sciences Naturelles 1956;18:569–668. Shine R. Reptilian reproductive modes: The oviparity– viviparity continuum. Herpetologica 1983;39:1–8. Sorci G, Clobert J. Natural selection on hatchling body size and mass in two environments in the common lizard (Lacerta vivipara). Evolutionary Ecology Research 1999; 1:303–16. Wake MH. Evolutionary scenarios, homology and convergence of structural specializations for vertebrate viviparity. American Zoologist 1992;32:256–63. Blackburn DG. Discrepant usage of the term ‘‘ovoviviparity’’ in the herpetological literature. Herpetogical Journal 1994;4:65–72. Lodé T. Reproductive strategies in animal kingdom (in French). Paris, France: Dunod-Masson Sciences; 2001. Wourms JP, Lombardi J. Reflections on the evolution of piscine viviparity. American Zoologist 1992;32:276–93. Busse K. Care of the young by male Rhimderma darwini. Copeia 1970;1970:395. Compagno LJV. Alternative life history styles of cartilaginous fishes in time and space. Environmental Biology of Fish 1990;28:33–75. Wourms JP, Grove BD, Lombardi J. The maternal–embryonic relationship in viviparous fishes. In: Hoar WS, Randall DJ, editors. Fish physiology. San Diego, USA: Academic Press; 1988. p. 1–134. Trexler JC, DeAngelis DL. Resource allocation in offspring provisioning: an evaluation of the conditions favoring the evolution of matrotrophy. American Naturalist 2003;162:574–85. Hedges SB, Duellman WE, Heinicke MP. New World direct-developing frogs (Anura: Terrarana): molecular phylogeny, classification, biogeography, and conservation. Zootaxa 2008;1737:1–182. Beck C. Mode of fertilization and parental care in anurans. Animal Behaviour 1998;55:439–49. Dumont JN, Brummett AR. Egg envelopes in vertebrates. Developmental Biology 1985;1:235–88. Hamlett WC, Koob TJ. In: Hamlett WC, editor. Sharks, skates, and rays: the Biology of Elasmobranch fishes. Baltimore, Maryland, USA: Johns Hopkins Univ Press; 1999. p. 398–443. Blackburn DG, Howard EE. Why are there no viviparous birds? American Naturalist 1986;128:165–90. Shine R. Does viviparity evolve in cold climate reptiles because pregnant females maintain stable (not high) body temperatures? Evolution 2004;58:1809–18. Nakaya K. Taxonomy, comparative anatomyand phylogeny of Japanese Catsharks scyliorhinidae. Japan: Hokkaido University; 1975. Andrew RM. Evolution of viviparity: variation between two sceloporine lizards in the ability to extend egg retention. Journal of Zoology 1997;243:519–95. Radder RS, Elphick MJ, Warner, Pike DA, Shine R. Reproductive modes in lizards: measuring fitness consequences of the duration of uterine retention of eggs. Functional Ecology 2008;22:332–9. Kupfer A, Müller H, Antoniazzi MM, Jared C, Greven H, Nussbaum RA, et al. Parental investment by skin feeding in a caecilian amphibian. Nature 2006;440:926–9. Gilmore RG. Reproductive biology of lamnoid sharks. Environmental Biology of Fishes 1993;38:95–114. Joung SJ, Hsu HH. Reproduction and embryonic development of the shortfin mako, Isurus oxyrinchus Rafinesque, 1810, in the northwestern Pacific. Zoological Studies 2005;44:487–96. Hamlett WC. Uterine specializations in elasmobranchs. Journal of Experimental Zoology 1998;282:438–59. 264 reproductive biology 12 (2012) 259–264 [36] Dantzer V, Paulesu L. Comparative biology of the vertebrate placenta – a workshop report. Placenta 1997;23:S133–5. [37] Angel F, Lamotte M. A viviparous toad in Western Africa Nectophrynoides occidentalis (Angel) (in French). Annales des Sciences Naturelles Zoologie 1944;6:63–89. [38] Jones RE, Gerrard AM, Roth JJ. Estrogen and brood pouch formation in the marsupial frog, Gastrotheca riobambae. Journal of Experimental Zoology 1973;184:177–84. [39] Lamotte M, Xavier F. Direct development anuran amphibians in Africa (in French). Bulletins de la Société Zoologique de France 1972;97:413–28. [40] Pino del E, Galarza M, Albura de C, Humphries AA. The maternal pouch and the development in the marsupial frog Gastrotheca, Fowler. Biological Bulletin 1975;149: 480–91. [41] Vilter V, Lugand A. Intrauterin trophism and embryo development in Nectophrynoides occidentalis Angel, totally viviparous, Nimba Montain, (Haute-Guinee) (in French). Comptes Rendus Académie des Sciences Biologies 1959;153:29–32. [42] Delsol M, Flatin J, Extrayat J-M, Bons M. Typhlonectes compressicaudus development (in French). Comptes-Rendus Académies des Sciences Biologies 1981;293:281–5. [43] Bailey RJ. The ovarian cycle in the viviparous teleost Xiphophorus hellen. Biological Bulletin 1933;64:206–25. [44] Mendoza G. The reproductive cycle of the viviparous teleost, Neotoca bilineata, a member of the family Goodeidae. I. The breeding cycle. Biological Bulletin 1939;76:359–70. [45] Shindler JF, Hamlett WC. Maternal–embryonic relations in viviparous teleosts. Journal of Experimental Zoology 1993;266:378–93. [46] Lodé T. Sex is not a solution for reproduction: the libertine bubble theory. BioEssays 2011;33:419–22. [47] El Albani A, Bengtson S, Canfield DE, Bekker A, Macchiarelli R, Mazurier A, et al. Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago. Nature 2005;466:100–4. [48] Solari AJ. Primitive forms of meiosis the possible evolution of meiosis. BioCell 2002;26:1–13. [49] Amoroso EC. The evolution of viviparity. Proceedings of the Royal Society of Medicine 1968;61:1188–200. [50] Kühnel S, Reinhard S, Kupfer A. Evolutionary reproductive morphology of amphibians: an overview. Bonn Zoological Bulletin 2010;57:119–26. [51] Stearns SC. The evolution of life histories. New York, USA: Oxford University Press; 1992.