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Mode of Reproduction: Invertebrate Animals

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From Subramoniam, T. (2018). Mode of Reproduction: Invertebrate Animals. In M. K. Skinner

(Ed.), Encyclopedia of Reproduction. vol. 6, pp. 32–40. Academic Press: Elsevier.
http://dx.doi.org/10.1016/B978-0-12-809633-8.20533-5
ISBN: 9780128118993
Copyright © 2018 Elsevier Inc. All rights reserved.
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Mode of Reproduction: Invertebrate Animals

Thanumalaya Subramoniam, Sathyabama University, Chennai, India
© 2018 Elsevier Inc. All rights reserved.

Introduction

Invertebrates represent the animal assemblage that lack true vertebral column. They are the most numerous kinds of living
animals, having marvelled the vertebrates by their sheer diversity of form and bodily organization. Whereas the basal metazoans
such as the sponges, cnidarians and flatworms are simple in organization, other invertebrate phyla, like Arthropoda, Mollusca,
and Echinodermata are much more complex, usually enveloped by armour-plated exoskeletons. Most invertebrates originated
and diversified in the sea, before some of them migrated to freshwater and then, species like insects, invaded terrestrial
environments. Their success in the colonization of every conceivable ecological niche both in water and on land is obviously
attributed to their various reproductive modes, ranging from the primitive vegetative binary fission to evolutionarily advanced
sexual reproduction.
Furthermore, this diversity in reproductive strategies could be correlated to the modes of development and life history patterns,
together with their ecological adaptiveness. In many invertebrates, the development is indirect with the interception of a larva,
which undergoes metamorphosis to reach the adult stage. Understandably, reproductive processes are inclusive of embryonic
development and larval metamorphosis in these forms. In marine invertebrates, the larvae are planktonic, playing a major role
in the dispersion of species, as the adults are normally sedentary, or sessile with limited mobility. Different types of larval forms
in marine invertebrates are listed in Table 1. In terrestrial and freshwater environments, however, pelagic larval development is
suppressed by virtue of the production of energy-rich yolky eggs, internal fertilization and sperm storage facility in the female.
Reproduction in protists is excluded in this article, as it involves mainly mitotic division of the whole body, thus differing vastly
from metazoan reproduction.

Asexual Reproduction

Although sex evolved early in animal evolution, agametic cloning from somatic tissue by asexual reproductive modes is prevalent in
most of the soft-bodied invertebrates such as sponges, cnidarians, flatworms, annelids, and some echinoderms, as well as
urochordates, a close relative of vertebrates. In sedentary corals, asexual reproduction is the clonal propagation in which an

Table 1 Larval forms of marine invertebrates

Phylum Class Larval forms

Porifera Parenchymula, Amphiblastula

Cnidaria Hydrozoa Planula, Actinula
Scyphozoa Planula, Actinula
Anthozoa Planula
Ctenophora Tentaculata Cydippid
Nuda Cydippid
Platyhelminthes Turbellaria Muller
Cestoda Miracidium, Cercaria
Trematoda Miracidium, Cercaria
Monogenea Onchomiracidium
Nemertea Pilidium
Annelida Polychaeta Trochophore, Nectochaeta
Mollusca Gastropoda Trochophore
Bivalvia Trochophore
Lophophorates Phoronida Actinula
Bryozoa Cyphonautes
Crustacea Copepoda Nauplius
Cirripedia Nauplius, Cypris
Malacostraca Zoea, Megalopa (Crab); Phyllosoma,
Puerulus (Lobster); Nauplius, Meta
nauplius, Mysis (Shrimp)
Echinodermata Echinoidea Pluteus
Asteroidea Dipleurula, Bipinnaria, Brachiolaria
Ophiuroidea Ophiopluteus
Holothuroidea Doliolaria
Hemichordata Enteropneusta Tornaria
Urochordata Tunicata Tadpole

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Table 2 Taxonomic distribution of asexual reproduction in invertebrates

Phylum Class Order Species

1. Agametic cloning
1a. Budding Placozoa Trichoplacoidea Trichoplacida Trichoplax adhaerens
Cnidaria Anthozoa Scleractinia Acropora palmata
Ctenophora Tentaculata Lobata Bolinopsis infundibulum
Xenacoelomorpha Acoela Convolutriloba macropyga
Convolutriloba retrogemma
Bryozoa Phylactolaemata Lophopus crystallinus
1b. Fission Placozoa Trichoplacoidea Trichoplacida Trichoplax adhaerens
1b. i. Binary fission (Simple) Echinodermata Asteroidea Forcipulatida Allostichaster polyplex
Cnidaria Anthozoa Actiniaria Haliplanella lineata
1b. ii. Transverse fission Xenacoelomorpha Acoela Convolutriloba hastifera
Convolutriloba longifissura
Platyhelminthes Rhabditophora Girardia tigrina
1b. iii. Longitudinal fission Annelida Oligochaeta Tubificida Paranais litoralis
Acoelomorpha Acoela Paratomella unichaeta
Platyhelminthes Rhabditophora Tubificida Planaria fissipara
1c. Fragmentation Ctenophora Tentaculata Lobata Mnemiopsis leidyi
Cnidaria Anthozoa Actiniaria Metridium senile
Nemertea Anopla Heteronemertea Lineus longissimus
Xenacoelomorpha Acoela Convolutriloba retrogemma
Hemichordata Enteropneusta Enteropneusta Balanoglossus capensi
2. Parthenogenesis Platyhelminthes Trematoda Echinostomia Philophthalmus megalurus
Rotifera Monogononta Ploimida Brachionus calyciflorus
Arthropoda Crustacea Cladocera Daphnia pulex
Arthropoda Insecta Hemiptera Myzus persicae
Hemiptera (Aphididea) Rhopalosiphum padi

organism gives rise to the production of genetically identical replicates (ramets) by budding. Conversely, unitary animals are those
that have a single body per genet (a genetic individual arising from one zygote by mitosis), which reproduce only sexually. Animals
that reproduce asexually are highly regenerative, compared to obligate sexual reproducers.
In invertebrates, adult stem cells play a pivotal role in regeneration and asexual reproduction. Unlike vertebrate systems,
invertebrate stem cells are not housed within a regulatory microenvironment (niche). Stem cells involved in agametic cloning in
invertebrate taxa are of different kinds: choanocytes in sponges; interstitial cells in cnidarians, neoblast cells in planarians, and
haemoblast stem cells in ascidians (Urochordata). Some metazoans like nematodes, rotifers, gastrotrichs and insects lack somatic
stem cells and hence the inability to undergo agametic cloning. Different kinds of asexual reproduction occurring in various
invertebrate animals are listed in Table 2.

Gemmule Formation in Sponges

All sponges (phylum Porifera) can regenerate their bodies and reproduce asexually using totipotent stem cells. In addition, many
freshwater sponges use choanocytes to develop dormant overwintering gemmules under unfavourable conditions. On return of
favourable conditions, such multicellular propagules reactivate and regenerate genetically identical replicas of the original sponge.

Fission, Budding and Fragmentation

In the simplest condition, asexual reproduction can take place by subdivision of an existing body into two or more multicellular
parts, followed by regeneration of the missing parts. Placozoans, the basal metazoan animals without distinct tissues or organs,
reproduce exclusively by fission, whereby two parts of the animal move away from each other until their connection is ruptured
(Fig. 1). In cnidarians, asexual reproduction is coupled with the sessile existence of the adult. In the freshwater hydrozoan, Hydra,
reproduction occurs almost exclusively by budding, suppressing gamete formation (Fig. 2). In the calyx region, the parent tissue
cells continuously move towards the bud-forming area and get incorporated into the growing bud. Evidently, reorientation and
repolarization of parent tissue play a major role in bud formation. In addition, epithelial stem cells that mediate the morphogenetic
plasticity of the tissue in regeneration may also have a similar role in asexual budding.
In Hydra, a new polyp bud eventually becomes a separate individual clone. However, in the coral relatives of Hydra, the clones do
not break off, but stay attached and become a branch as in plants. Such branching colonies are also found in the bryozoan,
Membranipora. In some anemones, the adults autotomise (self-mutilate) a tentacle, which regenerates in to a small individual. In
the scyphozoan cnidarian Aurelia, the polypoid scyphistoma undergoes horizontal fission (strobilation) into a stack of juvenile

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Fig. 1 Budding in Hydra vulgaris. Seen on the right side is a well grown bud and on the left, is early stage bud. Photo courtesy of Carolina
Biological Supply Company.

Fig. 2 Binary fission in the placozoan, Trichoplax. (a) Before fission, (b)–(d) Trichoplax progressing through asexual reproduction by fission.
Reproduced from Srivastava, M., Begovic, E., Chapman, J., et al., 2008. The Trichoplax genome and the nature of placozoans. Nature 454, 955–960.

medusas, called ephyra (Fig. 3). The ephyra transforms into male and female medusas, which produce planula larva by sexual
reproduction. The planula then settles into a sedentary scyphistoma, thus continuing the life cycle. This is termed as alternation
of generation or metagenesis. Whereas asexual reproduction produces genetically identical modules that may prolong the survival
of the genotype, sexual reproduction enables genetic recombination and production of new coral genotypes to enhance fitness and
survival of the species.
Scyphozoans also reproduce asexually by podocyst formation, under conditions of limited food supply. Podocysts are cysts
produced beneath the pedal discs of polyps of scyphozoans. They excyst small polyps that develop into active scyphistomae, which
are capable of producing further podocysts as well as medusas by strobilation.

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Fig. 3 Life cycle of Aurelia to demonstrate alternation of generation. Reproduced from Barnes, R.S.K., Calow, P., Olive, P.J.W, 1993. The
Invertebrates: A New Synthesis, second ed. Oxford: Blackwell Science Ltd., p. 488.

In the azooxanthellate soft corals, fragmentation of the colony occurs by autotomy. New clonal colonies in the reef corals are
also formed by colony fragmentation as a result of storm or wave impacts. In the anemone, longitudinal fission is the common
mode of asexual reproduction, although transverse fission occurs in some forms.
Asexual reproduction in sea anemones also occurs by basal laceration, which involves regeneration from a small piece of tissue
that typically includes all the three body layers. Different asexual modes of reproduction found in corals reflect the extraordinary
ability of cnidarian cell lines to differentiate, dedifferentiate and redifferentiate, providing their tissues with remarkable
developmental plasticity.
Budding is also common in flatworms (Platyhelminthes), which have excellent regenerative abilities. In the paratomic fission,
new individuals differentiate in a chain-like fashion from a parent worm before separating from it, while in architomy, the body
simultaneously fragments and only thereafter individuals differentiate from the pieces. The acoelous turbellarians release their
progeny by budding from the posterior margin of the body. In the nemertean worm, belonging to genus Lineus, sexually immature
adults undergo transverse fragmentation with subsequent regeneration. In the polychaete worm (Annelida), Dodecaceria, the adult
worm fragments into several individual segments, each of which reconstitutes a new head and a tail by renewed segment
proliferation.

Fissiparity and Budding in Echinoderms

The commonly occurring asexual mode of reproduction in sea stars and brittle stars is the division of the body across the disk,
termed fissiparity. Each resulting part regenerates a complete individual which can split again. The population of the fissiparous
sea star Coscinasteria stenuispina at Rio de Janeiro, Brazil, appears to be sustained only by fission, although these sea stars are capable
of gamete production. Another asexual method is autotomy, by which a whole new animal is regenerated from a single arm or even
part of an arm. Remarkably, fragmentation, fission or budding occur regularly in echinoderm larvae. Transverse fission has also been
reported in the sea cucumber, Holothuria edulis.
Both exogenous and endogenous factors appear to be involved in regulating asexual and sexual reproduction in echinoderms.
Whereas the asexual mode is related to small body size, sexual maturity is attained after an individual reaches a certain size.

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Regeneration after fission is aided by existing pluripotent stem cells or de-differentiation of tissues into stem cells. Conversely,
regeneration after autotomy, which takes place across predefined planes, involves the formation of an extensively proliferating
blastema. However, both these regenerative processes are nerve-dependent and require neurotransmitters and neuropeptides, as
growth factors.

Urochordates
The ascidian urochordates, sometimes called sea-squirts, are colonial marine invertebrates with remarkable budding capacity to
form new entities from existing structures. Two types of stem cells (epithelial and blood-born) are employed in the budding of
ascidians. Palleal budding (buds developed from thoracic body region) and stolonial budding (buds originating from distal tip
of developing stolon) are derivatives of epithelial stem cells, whereas in vascular budding, the buds are produced by the totipotent
haemoblast stem cells inside the vascular system.

Parthenogenesis
Parthenogenesis is the development of a new offspring from an unfertilized egg. Parthenogenetic lineages occur in many insect
species, but are widespread among other invertebrate taxa (Table 1). It entails modification or absence of meiosis so that the
eggs remain diploid and do not have to fuse with sperm to give rise to a diploid zygote. This kind of parthenogenesis is termed
as apomictic, which produces genetically identical modules of the same genet (typical asexual reproduction). In contrast, automixis
(meiotic parthenogenesis) restores diploidy by the fusion of the egg with the second polar body (e.g., free-living nematode,
Rhabditis). Obviously, the resultant modules may not be the exact genetic replicates of the mother.
In insects, parthenogenesis may be thelytokous (female producing), arrhenotokous (male producing) or amphitokous
(producing either sex). Haploid parthenogenesis is a special case in which the oocytes undergo regular meiotic division. If the
eggs are fertilized, the offspring is a female, and if the eggs remain unfertilized, then parthenogenetic development results in
a male offspring, which is haploid in its somatic tissues (e.g., the haplodiploid Hymenopteran insects). In social insects like the
subterranean termite, Reticuliter messperatus, the queens produce new queens asexually by thelytokous parthenogenesis, but produce
other colony members (workers and soldiers) by sexual reproduction. The parthenogenetic production of these new queens is
achieved by the closing of the egg’s micropyle (sperm gates) to prevent sperm entry. Yet another type, namely obligate
parthenogenesis, occurs in bdelloid rotifers, in which sexual reproduction never takes place due to the lack of males in the
population.
In the cladoceran rotifers and aphid insects, parthenogenesis occurs cyclically together with bouts of sexual reproduction. This is
called cyclical parthenogenesis. In Daphnia, parthenogenetic reproduction takes place for one to several generations during
favourable conditions, followed by sexual reproduction under unfavourable environments. The sexually produced long-lived
dormant eggs hatch once favourable conditions return. By this alternation of generations, favourable environmental conditions
can be exploited to increase the number of offspring by parthenogenetic reproduction, whereas the periodical appearance of one
or more sexual generations will ensure genetic advantages such as increased heterosis, and re-assortment of genetic characters.

Sexual Reproduction

Sexual reproduction involves haploid gamete formation and their subsequent fusion (amphimixis), paving the way for genetic
recombination in the newly formed genotypes to enhance fitness and survival. Over 99% of all invertebrates exhibit sexual
reproduction at some stage in their lives. Sexuality has evolved early in basal metazoans like placozoans by the formation of gametic
cells, even before the origin of a discrete gonad. At this level of sex cell origin, certain stem cell-like choanocytes (sponges) and
interstitial cells (cnidarians) could give rise to or differentiate into both egg and sperm. In the flatworms, the gametes are loosely
spread among the mesenchyme cells. Only in the coelomate invertebrates, true gonads are formed to give rise to sperm and eggs.
Thus, in the majority of invertebrate animals, sexual reproduction is the main mode for the propagation of progeny.

Sexual Systems
Invertebrates have undergone dynamic species radiation, occupying diverse niches in both aquatic and terrestrial ecosystems. The
correlated diversity in their morphological features and physiological adaptations has given origin to an array of sexual systems and
reproductive modalities. Their highly variable patterns of reproduction have an underlying relationship with the manner in which
sex determination and differentiation have taken place in different invertebrate taxa.
Although gonochorism (separate sex) is the principal mode of sexuality in invertebrates, alternative sexual systems also exist in
the form of mixed-sex hermaphrodites (same sex). A hermaphrodite is an individual that produces functional male and
female gametes in its lifetime. Approximately 65,000 species (about 6%) of known invertebrate animals are hermaphroditic
with representation in nearly 50% of 85 invertebrate classes (Table 3). Unlike plants, hermaphroditism is considered to be a derived
condition in invertebrate lineages. Using phylogenetic character mapping, it has been deduced that hermaphroditism is
polyphyletic in invertebrate animals, having arisen from ancestral gonochorism on many separate occasions.
Hermaphroditism is rarely reported in insects, but crustaceans possess various categories of sexual systems (Table 4). Primitive
groups of crustaceans such as notostracans and conchostracans show an extensive variation in their reproductive strategy that

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Table 3 On the occurrence of hermaphroditism among invertebrate animals

Phylum Lower taxon Popular name Hermaphroditism

Porifera Sponges Ubiquitous

Cnidaria Hydrozoa Hydras and hydroids Rare
Scyphozoa and Cubozoa Jellyfish Rare
Anthozoa Anemones and corals Ubiquitous
Annelida Polychaeta Rare
Pogonophora Rare
Gnathostomulida Ubiquitous
Oligochaeta Earthworms, freshwater oligochaetes Ubiquitous
Hirudinea Leeches Ubiquitous
Arthropoda Crustacea Crabs, shrimps, crayfish, woodlice, Rare
copepods, barnacles
Tardigrada Water bears Rare
Sipunculida Peanut worms Rare
Ectoprocta Bryozoans Ubiquitous
Platyhelminthes Cestoidea Tapeworms Ubiquitous
Trematoda Flukes Ubiquitous
Monogenea Monogenean ectoparasites Ubiquitous
Turbellaria Free-living flatworms Ubiquitous
Nemertini Ribbon worms Rare
Chaetognatha Arrow worms Ubiquitous
Gastrotricha Ubiquitous
Nematoda Round worms Present
Ctenophora Sea walnuts, comb jellies Ubiquitous
Phoronidea Present
Brachiopoda Lamp shells Rare
Echinodermata Starfish, brittle stars, sea urchins, Rare
sea cucumbers, sea lilies
Urochrodata Sea squirts, salps Ubiquitous

Source: Modified from Michiels, N.K., 1998. Mating conflicts and sperm competition in simultaneous hermaphrodites. In: Birkhead, T.R.,
Møller, A.P. (Eds.), Sperm Competition and Sexual Selection. London: Academic Press, pp. 219–248 and Avise, J., 2011.
Hermaphroditism: A Primer on the Biology, Ecology, and Evolution of Dual Sexuality. New York, NY: Columbia University Press.

may range from gonochorism to self-fertilizing hermaphroditism and parthenogenesis. The transition from gonochorism to
hermaphroditism is also evident in the clam shrimp Eulimnadia (Conchostraca: Crustacea) by the occurrence of an extreme sexual
type, androdioecy. Interestingly, the hermaphrodites of clam shrimp lack clasping appendages for mating and thus can only
self-fertilize or mate with males. In malacostracan crustaceans, androgenic gland hormone controls sex differentiation and
causation of different hermaphroditic conditions.
Among the various forms of mixed sex forms, simultaneous and sequential hermaphroditism is most common. Simultaneous
hermaphrodite is an animal that produces ripe sperm and ova at the same time. Although self-fertilization (selfing) is possible in
many simultaneous hermaphrodites, offering fertilization assurance, many invertebrates practise cross fertilization in order to gain
genetic variability among the resultant offspring. The major genetic deterrent to selfing is however inbreeding depression. Therefore,
many species of simultaneously hermaphroditic invertebrates have evolved genetic self-incompatible systems that inhibit
self-fertilization. Sequential or successive hermaphroditism is another form of hermaphroditism, commonly found among
invertebrates like corals, molluscs and crustaceans. Here, the individual produces both male and female gametes at different periods
of its life. They are either male or female at a time with a brief transitional state, called ‘intersexual’ during the changeover phase.

Mating Systems
Mating brings together both male and female gametes, culminating in fertilization and production of a diploid zygote. In marine
invertebrates, such as cnidarians, polychaetes, and echinoderms, broadcast spawning and external fertilization is the rule, favoured
by the seawater medium that could support prolonged gamete survival, fertilization and early development. For example, in the
reef-building corals that live in shallow waters of the tropical oceans, both gonochoristic and hermaphroditic species release the
gametes into the open sea, where random mating (fusion of gametes) occurs. The fertilized eggs undergo development to release
the planktonic planula larvae, which are dispersed to far-away locations for settlement. Both external fertilization and the
possession of pelagic larvae in many marine invertebrates are considered to be a primitive pattern of reproduction, with a clear
advantage of colonizing new habitats. Alternatively, internal fertilization, followed by brooding of the planula larvae within their
polyps also takes place in gonochoristic and simultaneously hermaphroditic anthozoan corals. The brooded larvae released from
the coral polyp search for a suitable site in the reef substratum for attachment and metamorphosis into a juvenile polyp.

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Table 4 Different types of sexual systems present in crustaceans

Types of sexuality Developmental sequence Examples

Gonochorism Juvenile ~
x Primary male Brachyuran crab – Scylla serrata
Juvenile ~
x Primary female
Androdioecy Juvenile ~
x Primary male Clam Shrimp – Eulimnadia texana
Juvenile ~
x Hermaphrodites
Sequential hermaphroditism Juvenile ~
x Male phase ~ x Female phase Humpy shrimp – Pandalus goniurus
a.Simple protandry Juvenile ~
x Male phase ~ x Female phase Palaemonid shrimp – Processa edulis
b.Protandry (with primary females) Juvenile ~
x Primary female
c.Protandry (with early maturing Juvenile Male phase Female phase Pink shrimp – Pandalus borealis
females) “early maturing” female phase
d.Protogyny Juvenile ~
x Female phase ~ x Male phase Isopod – Cyanthura carinata
Simultaneous hermaphroditism Juvenile ~
x Both functional male and female in the same Mud shrimp – Calocaris macandrae
individual
Protandric simultaneous Juvenile ~
x Male phase ~ x Simultaneous hermaphrodites Monaco Shrimp – Lysmata seticaudata
hermaphroditism
Intersexuality
a.Normal intersexuals (existing as a Juvenile Male phase Intersexuals Crayfish – Parastacus varicosus
part of life cycle) (Transitory)

Female phase
(as in protandric hermaphroditism)
Juvenile Female phase Intersexuals Isopod – Cyanthura carinata
(Transitory)

Male phase
(as in the case of protogyny)
Juvenile ~
x Male phase ~ x Intersexuals Amphipod – Gammarus deubeni
(due to incomplete feminization by parasites)
b.Epigenetic intersexuals (arising Juvenile ~
x Female phase ~ x Intersexuals Blue crab – Calinectus sapidus
from epigenetic factors) (due to androgenic gland implants)
c.Sex intermediates Juvenile ~
x Sex intermediates Cladocera – Daphnia pulex
(hormonal disruption by methyl farnesoate)
d.Gynandromorphism Embryo ~ x Bilateral gynandromorphism Brine shrimp – Artemia franciscana
(due to the chromosomal mutation in the early embryonic
stage)
Embryo ~ x Bilateral gynandromorphism Lobster – Homarus gammarus
(due to chromosomal loss during early embryonic
cleavage)

Source: Data based on Subramoniam, T., 2016. Sexual Biology and Reproduction in Crustaceans. London: Academic Press/Elsevier, p. 526.

Sperm Transfer Mechanisms

In terrestrial and freshwater invertebrates, release of unprotected sperm and egg into the medium is unsafe and hence fertilization
must be internal, requiring direct pairing between male and female partners, often associated with complex copulatory behav-
iour. A feature associated with internal fertilization in invertebrate animals is the formation of sperm packets, called spermato-
phores, which prevent sperm loss during copulation. In the primitive insects and other cryptozoic arthropods, however,
spermatophores seem to have evolved prior to the development of copulatory organs, as a means to transfer semen to effect indi-
rect, contact-free transfer from male to female. In the more advanced insects, the spermatophores are replaced by liquid semen,
transferred by well-formed penes. Spermatophores have also evolved independently in aquatic invertebrates such as crustaceans
and mollusks in which they are deposited externally onto the female body or inserted into the seminal receptacles by way of copu-
latory organs.
Indirect sperm transfer has also been encountered in soil-dwelling polychaetes, semi terrestrial oligochaetes and leeches. In the
hermaphroditic rhynchobdellid leeches, the tubular spermatophores are attached to the skin of their partners along with a hydrolytic
secretion. The contraction of the spermatophore injects the sperm into the body cavity, where they reach the eggs by chemotaxis.
Hypodermic insemination has also been reported in the onychophore, Peripatus, hermaphroditic sea slug, and some flatworms.

Mating Behaviour
Several mating behaviours have evolved in invertebrate animals in accordance with the modes of sperm transfer, the lifestyles and
habitat conditions. Chemical communication by way of pheromones is also involved in the attraction of mates and the ensuing

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courtship. Olfactory sex pheromones involved in the attraction of male moths over greater distances are well-known. Marine
invertebrates release a water-soluble pheromone bouche to attract the opposite sex for mating and sperm transference. In the marine
polychaetes, the swarming of epitokous (sexually mature) heteronereids is effected by the pheromone, inducing a nuptial dance and
gamete release for external fertilization. Marine crustaceans such as the lobsters, crayfish and crabs, also use pheromones for
communication and coordination of sexual activities.

Alternative Mating Strategy

Several studies have described variation in male mating behaviour among invertebrate animals. Any deviation from their common
mating behaviour is considered as alternative mating strategy. In males, such deviant behaviours are associated with the assumption
of reproductive phenotypes or morphotypes. Alternative mating strategy has apparently evolved in response to variation in the
mating environment. The marine isopod Paracerceis sculpta, which breeds inside the spongocoel, has three genetically distinct
male morphotypes, a male, b male, and g male. The largest and dominant a male possesses elongated uropods and defends harems
within the spongocoel. The smaller b males resemble females morphologically and invade the spongocoel by mimicking female
behaviour. The g male is tiny and adopts sneak mating tactics to gain access to females. The occurrence of dwarf males has been
reported in many invertebrate species, in which they adopt several alternative mating strategies.

Types of Mating and Social Organization

Mating system refers to the procedures used in finding and securing a mate, the number of mates an individual acquires, the type of
pair bonds, and the nature of parental care. The basic mating systems found in invertebrates are monogamy and polygamy.
Although such mating behaviours have evolved in vertebrates to a high level, higher invertebrate groups like arthropods and
molluscs practise them along with other behavioural traits such as parental care. Monogamy has been practised even among the
hermaphroditic pair of a tube-dwelling polychaete worm, Ophryotrocha diadema, which lives together for several reproductive cycles.
Mating events consist of one partner spawning eggs and the other fertilizing them. In this case of ‘egg trading’ both partners share
brood care.
As in birds, social monogamy in certain coral-reef dwelling caridean shrimps has evolved into territorial cooperation and
extended mate guarding by the male partner. In many crustaceans, mating occurs in the fresh moult stage when the female is
receptive to males. Hence a new behavioural trait, namely pre-copulatory mate guarding by the males has evolved as a physiological
necessity. Interestingly, in the sponge-dwelling snapping shrimp Synalpheus, social monogamy has given origin to advanced social
systems, such as eusociality. Among other invertebrates, reproductive division of labour and cooperative care of young, resulting in
eusocial condition has been well-defined only in social insects like honey bees and termite ants.

Unusual Reproductive Strategies

Polyembryony
Polyembryony, otherwise known as embryonic cloning, refers to the splitting of one sexually produced embryo into many offspring,
which are genetically identical to each other but distinct from their parent(s), thus differing from asexual budding. Polyembryony
occurs in a wide range of invertebrates, like cnidarians, bryozoans, insects and echinoderms (Table 5). In the cyclostome Bryozoa,
cloning occurs by fission of blastula-stage embryo, with each blastomere becoming an individual offspring. In the classic example of
the parasitic hymenopteran insects, the female wasp, Copidosma, oviposits one or two eggs inside the moth egg, which develops
subsequently into a caterpillar larva. Inside the moth larva, the wasp’s egg develops into a single compact mass of cells, called
morula, which fragments into a large number of diminutive units that develop into two types of larvae. One type develops into
a normal fertile adult, while the other type, called soldier larva, has a thin worm-like body, and becomes sterile.

Viviparity
In the great majority of invertebrate species, females lay eggs that develop and hatch in the external environment (oviparity).
However, in some species females retain fertilized eggs inside the body and give birth to the young (viviparity). In the pulmonate
terrestrial snails, viviparity exists in two forms: lecithotrophic viviparity (embryonic nutrition from egg yolk) and matrotrophic
viviparity (nutrients supplied by maternal tissue). All species of scorpions are viviparous and the offspring are directly nourished
by the mother during development. The young escape through the gonopore and crawl on to the mother’s back for protection
and parental care.
Insects are known to display various viviparous developments, but in a strange reproductive mode, termed hemocoelic
viviparity, embryonic development occurs in the hemocoel of the mother, obtaining nutrients through their egg membrane by
osmosis. In an interesting example, a parasitic female wasp injects her eggs into the ladybug. The eggs hatch and the larvae feed
on the interior of the host insect. When the larva is ready to transform into a wasp, it comes out of the ladybug’s abdomen and
spins a cocoon, which is guarded by the ladybug from predators.

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40 Modes of Reproduction j Mode of Reproduction: Invertebrate Animals

Table 5 Occurrence of polyembryony in invertebrates

Phylum Class Order Species

Cnidaria Hydrozoa Trachylina Pegantha spp.

Cunina spp.
Hydroida Cunoctantha spp.
Polypodium hydriforme
Platyhelminthes Monogenea Gyrodactyloidea Gyrodactylus elegans
Cestoidea Eucestoda (subclass) Echinococcus spp.
Trematoda Digenea (subclass) Schistosoma spp.
Arthropoda Cirripedia (Crustacea) Rhizocephala Loxothylacus panopaei
Insecta Hymenoptera
– Encyrtidae Copidosoma spp.
– Platygastridae Platygaster spp.
– Braconidae Macrocentrus spp.
– Dryinidae Macrocentrus spp.
Strepsiptera Halictoxenos simplicis
Bryozoa Stenolaemata Cyclostomata All species studied to date
(e.g., Crisia spp.)
Echinodermata Asteroidea Paxillosida Luidia sp.
Unidentified non-paxillosid
Ophiuroidea Ophiurida Ophiopluteus opulentus

Paedogenesis
In this reproductive mode, viviparity and neoteny (attainment of sexual maturity in larva) are combined. In the paedogenic insects,
the ovaries of larvae become active and the eggs develop parthenogenetically. Paedogenesis often occurs in parasitoids, which live in
the hemocoel of a host insect. Free-living insects (Homoptera) also exhibit paedogenesis. Here, the parthenogenetically developing
larvae within the ovarioles of the mother contain embryos, so that a female aphid will contain her own grand-daughters.

Conclusion

The diversity in form and anatomical features of reproductive functions is truly reflected in the exhibition of numerous reproductive
modes in invertebrate animals. The absence of phylogenetic relatedness in the occurrence of different reproductive strategies may
imply their independent evolutionary origin among various invertebrate species. Nevertheless, the predominance of vegetative
reproductive methods, ubiquitous or alternative to sexual propagation, furthermore indicates the co-evolution of both asexual
and sexual reproductive processes in exploiting the environmental conditions. Another aspect of asexual reproduction in
invertebrates is the occurrence and active participation of adult stem cells in agametic cloning of both colonial and unitary species
such as the cnidarians. In Hydra vulgaris, induction of sexual reproduction leads to senescence and early death, whereas maintenance
of asexual reproduction does not show any sign of aging. Constant self-renewal of stem cells during asexual reproduction and the
loss of interstitial stem cells during gametogenesis are the proposed reasons for the above differences in their longevity. Stem cells of
invertebrates demonstrate alkaline phosphatase activity (a marker of embryonic stem cells in vertebrates) and express vasa-like genes
(as expressed in primordial germ cells), underpinning their importance in the evolution of asexual reproductive processes among
various taxa. Significantly, invertebrate stem cells could become vital model systems to investigate molecular mechanisms
underlying ageing and longevity in higher animals, including humans.
In invertebrates, sexual reproductive processes appear to be strongly influenced by various environmental factors. In particular,
gametogenic cycles are initiated and synchronised with environmental changes by extrinsic or exogenous factors. In consequence,
synchronised spawning within coral population enhanced fertilization success leading to increased planula production. For the
marine invertebrates, seasonal changes in sea temperature, day length, wind or current patterns, lunar cycles or night irradiance
are the major environmental factors to control reproduction and spawning. In terrestrial invertebrates like insects, a variety of
extrinsic variables such as temperature, photoperiod, humidity, and food availability may influence egg production and fecundity.
The retention of primitive reproductive characteristics such as external fertilization and the development of planktonic larva in
marine invertebrates demonstrate their evolutionary origin in the sea, which has changed little in physical and chemical properties
since life began in it. Any change in the chemistry of seawater due to the predicted climate change could adversely affect
reproduction in marine invertebrates. Conversely, terrestrialization has necessitated the development of certain modified
reproductive traits such as sperm transfer via spermatophores, sperm storage in females, internal fertilization and the production
of yolk-rich eggs. In spite of the widespread occurrence of sexual reproduction, invertebrates have effectively combined this
mode with episodes of asexual reproduction in their complex life cycles.

Encyclopedia of Reproduction, Second Edition, 2018, 32–40

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