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reproductive biology 12 (2012) 259–264
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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
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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
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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.
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