251
Brief colony life is also characteristic of the hippothoid
Celleporella hyalina (Eggleston 1972 ). These observations
are in accord with recently discussed data on poeciliid fi shes
in which placentation is associated with an increase in the
rate of production of offspring early in life (Pires et al.
2011 ). However, many cheilostome species with ephemeral
colonies have no embryophore (Ostrovsky 1998c , 2009 ,
2013 ; Ostrovsky et al. 2009a ; Moosburgger et al. 2012 ) and
there are some matrotrophic species with long-lived, heavily calcifi ed colonies (e.g. Myriapora truncata , species of
Adeonidae and some other families).
3.3.6 Prerequisites and Role of Embryo
in Evolution of Matrotrophy
The origin of EEN in Cheilostomata became possible only
after complete isolation of the incubatory space from the
external medium. This condition was also considered to be
indispensable for the evolution of matrotrophy in bivalves
(see Richard et al. 1991 ). Another prerequisite was the permeability of at least part of the wall of the brood chamber to
low-molecular substances, allowing their bidirectional
transport.
In the experiments of Silén ( 1945 ), embryos of the nonmatrotrophic cheilostome Callopora dumerilii rapidly died
after being transferred from ovicells to sea water. Thus, the
fl uid in the brood chamber, the cavity of which is topologically exterior, appears to be considerably different from seawater, being probably chemically infl uenced by the maternal
zooid via the non-calcifi ed wall of the ooecial vesicle.
Osmoregulatory and excretory relationships involve
active maintenance of the periembryonic environment via
physiological mechanisms during incubation (Lombardi
1998 ). The developing embryo is metabolically active, and
one can speculate that the transport of small molecules
occurs in both directions (for instance, simple sugars and
amino acids from the coelomic fl uid of the fertile zooid to the
brood chamber and excretory metabolites from the fl uid of
the brood cavity back to the visceral coelom). This may have
initially been a passive mechanism, driven by concentration
gradients together with gas exchange. Since hypertrophy of
the embryophore cells in matrotrophic bryozoans occurs
only when the embryo is in the brood chamber, it is likely
that a direct chemical infl uence (signal) causes changes in
the embryophore cells, stimulating their hypertrophy. One
may speculate that their increased size and activity refl ects
an “attempt” to blockade/neutralize the excretory metabolites of the embryo by producing substances that afterwards
became a source of nutrition for it. Even if this is not the
case, it can be assumed that EEN is a by-product of the
chemical relationship between the developing embryo and
its “parent”. On the other hand, the infl uence of the embryo
does not result in the formation of placental analogues in
most cheilostome brooders studied. It is especially intriguing
that both variants have been found in species of the same
genus Catenicella .
3.3.7 Matrotrophy and Evolution of Sexual
Polymorphism in Cheilostomata
It seems that the evolution of matrotrophy could have induced
zooidal sexual polymorphism. Harmer ( 1926 ) suggested that
the change from brooding in ovicells to incubation in an
internal sac “has probably been induced by the supply of an
increased amount of nutrient yolk to the embryo” (p. 254).
Although the transition from external to internal brooding in
some families was probably associated with better embryonic protection (see Ostrovsky et al. 2006 , 2007 , 2009b ),
matrotrophic incubation inside a voluminous zooid might
have resulted in additional embryonic enlargement. Thus,
matrotrophy may have facilitated the origin of sexual polymorphism since many, if not all, species in the cheilostome
family Adeonidae (presumably entirely placentotrophic) are
characterized by larger orifi cial size and, in many instances,
enlarged brooding zooids. Similarly, EEN might have
resulted in the evolution of polyembryony and enlarged
gonozooids in the bryozoan class Stenolaemata (Ostrovsky
2013 ) and female zooids in Epistomia .
3.3.8 Distribution of Placentotrophy
in Bryozoa
While modes of EEN have been thoroughly reviewed in vertebrates (Wourms 1981 ; Wourms et al. 1988 ; Wourms and
Lombardi 1992 ; Blackburn 1992 , 1999b , 2005b ; Blackburn
et al. 1985 ; Wooding and Burton 2008 ), there has been no
attempt to review the topic in invertebrates. Modes of matrotrophy occurring during embryonic incubation include oophagy,
adelphophagy,
histotrophy,
histophagy,
and
placento trophy (modifi ed from Wourms 1981 and Blackburn
et al. 1985 ; Blackburn 1999b ). Chordates possess all these
modes, with placentotrophy commonest. It exists in mammals (except monotremes), many squamate reptiles, a relatively large number of bony and cartilaginous fi shes, some
ascidians and all salps (Wourms 1981 ; Mukai et al. 1987 ;
Godeaux 1990 ; Blackburn 1993 ; 2005a , b ; Wooding and
Burton 2008 ). An equivalent variety is found among invertebrates, but histotrophy is the commonest mode. Placentotrophy
evolved in Porifera, Cestoda, Scorpiones, Insecta, Gastropoda,
Onychophora, Kamptozoa and Bryozoa (Ereskovsky 2010 ;
Hagan 1951 ; Anderson 1973 ; Tompa 1984 ; Nielsen 1990 ;
Reed 1991 ; Farley 2001 ; Korneva 2005 ), but in most of these
groups there are only a few placental species. In contrast,
scorpions (currently more than 1,700 species) are, apparently, all placentotrophic (Farley 2001 ). “Pseudoplacental
3.3 Evolution of Matrotrophic Incubation in Cheilostomata
Brief colony life is also characteristic of the hippothoid
Celleporella hyalina (Eggleston 1972 ). These observations
are in accord with recently discussed data on poeciliid fi shes
in which placentation is associated with an increase in the
rate of production of offspring early in life (Pires et al.
2011 ). However, many cheilostome species with ephemeral
colonies have no embryophore (Ostrovsky 1998c , 2009 ,
2013 ; Ostrovsky et al. 2009a ; Moosburgger et al. 2012 ) and
there are some matrotrophic species with long-lived, heavily calcifi ed colonies (e.g. Myriapora truncata , species of
Adeonidae and some other families).
3.3.6 Prerequisites and Role of Embryo
in Evolution of Matrotrophy
The origin of EEN in Cheilostomata became possible only
after complete isolation of the incubatory space from the
external medium. This condition was also considered to be
indispensable for the evolution of matrotrophy in bivalves
(see Richard et al. 1991 ). Another prerequisite was the permeability of at least part of the wall of the brood chamber to
low-molecular substances, allowing their bidirectional
transport.
In the experiments of Silén ( 1945 ), embryos of the nonmatrotrophic cheilostome Callopora dumerilii rapidly died
after being transferred from ovicells to sea water. Thus, the
fl uid in the brood chamber, the cavity of which is topologically exterior, appears to be considerably different from seawater, being probably chemically infl uenced by the maternal
zooid via the non-calcifi ed wall of the ooecial vesicle.
Osmoregulatory and excretory relationships involve
active maintenance of the periembryonic environment via
physiological mechanisms during incubation (Lombardi
1998 ). The developing embryo is metabolically active, and
one can speculate that the transport of small molecules
occurs in both directions (for instance, simple sugars and
amino acids from the coelomic fl uid of the fertile zooid to the
brood chamber and excretory metabolites from the fl uid of
the brood cavity back to the visceral coelom). This may have
initially been a passive mechanism, driven by concentration
gradients together with gas exchange. Since hypertrophy of
the embryophore cells in matrotrophic bryozoans occurs
only when the embryo is in the brood chamber, it is likely
that a direct chemical infl uence (signal) causes changes in
the embryophore cells, stimulating their hypertrophy. One
may speculate that their increased size and activity refl ects
an “attempt” to blockade/neutralize the excretory metabolites of the embryo by producing substances that afterwards
became a source of nutrition for it. Even if this is not the
case, it can be assumed that EEN is a by-product of the
chemical relationship between the developing embryo and
its “parent”. On the other hand, the infl uence of the embryo
does not result in the formation of placental analogues in
most cheilostome brooders studied. It is especially intriguing
that both variants have been found in species of the same
genus Catenicella .
3.3.7 Matrotrophy and Evolution of Sexual
Polymorphism in Cheilostomata
It seems that the evolution of matrotrophy could have induced
zooidal sexual polymorphism. Harmer ( 1926 ) suggested that
the change from brooding in ovicells to incubation in an
internal sac “has probably been induced by the supply of an
increased amount of nutrient yolk to the embryo” (p. 254).
Although the transition from external to internal brooding in
some families was probably associated with better embryonic protection (see Ostrovsky et al. 2006 , 2007 , 2009b ),
matrotrophic incubation inside a voluminous zooid might
have resulted in additional embryonic enlargement. Thus,
matrotrophy may have facilitated the origin of sexual polymorphism since many, if not all, species in the cheilostome
family Adeonidae (presumably entirely placentotrophic) are
characterized by larger orifi cial size and, in many instances,
enlarged brooding zooids. Similarly, EEN might have
resulted in the evolution of polyembryony and enlarged
gonozooids in the bryozoan class Stenolaemata (Ostrovsky
2013 ) and female zooids in Epistomia .
3.3.8 Distribution of Placentotrophy
in Bryozoa
While modes of EEN have been thoroughly reviewed in vertebrates (Wourms 1981 ; Wourms et al. 1988 ; Wourms and
Lombardi 1992 ; Blackburn 1992 , 1999b , 2005b ; Blackburn
et al. 1985 ; Wooding and Burton 2008 ), there has been no
attempt to review the topic in invertebrates. Modes of matrotrophy occurring during embryonic incubation include oophagy,
adelphophagy,
histotrophy,
histophagy,
and
placento trophy (modifi ed from Wourms 1981 and Blackburn
et al. 1985 ; Blackburn 1999b ). Chordates possess all these
modes, with placentotrophy commonest. It exists in mammals (except monotremes), many squamate reptiles, a relatively large number of bony and cartilaginous fi shes, some
ascidians and all salps (Wourms 1981 ; Mukai et al. 1987 ;
Godeaux 1990 ; Blackburn 1993 ; 2005a , b ; Wooding and
Burton 2008 ). An equivalent variety is found among invertebrates, but histotrophy is the commonest mode. Placentotrophy
evolved in Porifera, Cestoda, Scorpiones, Insecta, Gastropoda,
Onychophora, Kamptozoa and Bryozoa (Ereskovsky 2010 ;
Hagan 1951 ; Anderson 1973 ; Tompa 1984 ; Nielsen 1990 ;
Reed 1991 ; Farley 2001 ; Korneva 2005 ), but in most of these
groups there are only a few placental species. In contrast,
scorpions (currently more than 1,700 species) are, apparently, all placentotrophic (Farley 2001 ). “Pseudoplacental
3.3 Evolution of Matrotrophic Incubation in Cheilostomata