246
embryophore to one that was active, and thus from incipient
to substantial placentotrophy. The redistribution of the load
was refl ected in the structure of the ovary – fi rst of all, in the
number and size of its cells. Oocytes gradually became
smaller, accumulated less yolk and began to ripen faster.
A commonly accepted scenario for the evolution of
matrotrophy is based on the development of viviparous vertebrates (see Packard et al. 1977 ; Blackburn 1992 , 1993 ,
1999a , 2005a , 2006 ). In this case, internal fertilization and
retention of eggs are the major preconditions. Primitive fetal
nutrition would have been strictly lecithotrophic and developed further by the addition of small quantities of nutrients
from the reproductive tract of the viviparous female. This
so-called “incipient matrotrophy” is considered to have been
an initial step towards the evolution of the “specialized”
(Wourms 1981 ) or “substantial matrotrophy” (Blackburn
1992 ) that was accompanied by a subsequent shift in oogenesis. Examples corresponding to this scenario have been
thoroughly studied in squamate reptiles (reviewed in
Blackburn 1992 ) and poeciliid fi shes (Reznick et al. 2002 ;
Pollux et al. 2009 ; reviewed in Wourms 1981 ; MarshMatthews et al. 2010 ). When we deal with placenta-like systems, the term “incipient placentotrophy” can be applied
(Blackburn 1993 , 2005a , b ).
As for invertebrates, incipient matrotrophy (and sometimes placentotrophy) almost certainly exists among
onychophorans (Anderson 1973 ), scorpions (Farley 2001 )
and insects (Hagan 1951 ), although no defi nitive statements
concerning this phenomenon have been made.
My results indicate that both incipient and substantial
placentotrophy is present among cheilostome bryozoans.
Moreover, the fi nding of different modes of oogenesis and
degrees of embryonic enlargement and embryophore development in a variety of species (see Sects. 1.2.5 and 1.2.6 )
gives insight into the scenario(s) of transition from one of
these nutritional modes to the other. Considering cheilostomes with reproductive pattern IV fi rst, small placental
analogues (embryophores) have been recorded in four species with large macrolecithal oocytes that are slightly smaller
than the brood cavity or comparable in size to it ( Klugefl ustra
antarctica , Isosecurifl ustra angusta , Micropora notialis and
Figularia fi gularis ). Slight/negligible (ca 1.5-fold) enlargement of the embryo in them suggests a small nutrient supply.
Ultrastructural or experimental evidence is missing and it is
possible that EEN is absent. Hypertrophy and increase in the
number of embryophore cells together with the change in the
staining of their cytoplasm might then be explained, for
instance, by active gas exchange or/and removal of waste
material from the brood chamber. The most important sign
of a maternal-fetal physiological relationship is a recognizable response of the maternal cells to the appearance of a
zygote in the brood chamber, which points to molecular
transport. Even if EEN is absent, the establishment of such a
relationship can be the basis for further acquisition of
matrotrophy. In passing, it may be noted that mother-toembryo nutrient transfer has been recorded in experiments
involving a number of poeciliid teleost fi shes with large
yolky eggs (Marsh-Matthews et al. 2010 ).
In three species ( Cellaria tenuirostris , Cribricellina
cribraria and Watersipora subtorquata ) with the same reproductive pattern (IV), the embryo becomes noticeably larger
(3–3.39-fold increase) in comparison with mature macrolecithal eggs, despite hypertrophy of the embryophore cells
in these species being rather modest. Thus, a degree of morphological development of the placental analogue is not necessarily directly correlated with its nutritive activity.
Elaboration of placental structures has been known to correlate with a degree of nutritional provisioning during gestation in teleost fi shes (Turner 1940 ) and some scinks
(Flemming and Blackburn 2003 ), but my data show that it is
not always the case in cheilostomes (Ostrovsky 2013 ).
In six other cheilostomes (pattern IV, Beania bilaminata ,
Bicellariella ciliata , Celleporella hyalina , “ Calyptotheca ”
variolosa , Costaticella solida , C . bicuspis ), embryo enlargement is substantial or even very substantial and comparable
with that in species with pattern III [Despite the absence of
late embryos in available colonies C . bicuspis , a welldeveloped embryophore and the size difference between the
early embryo and the brood cavity allows for the inclusion of
this species here]. Actually, except for differences in mode of
oogenesis (macrolecithal vs oligolecithal), these two reproductive variations are identical, both involving an embryophore with strongly hypertrophied cells and eggs that are
considerably smaller than the brood cavity (Moosburgger
et al. 2012 ; Ostrovsky 2013 ).
Based on this information, it might be suggested that a
combination of large macrolecithal oocytes comparable in
size to that of the brood cavity, and minimal embryonic
enlargement provided by a small embryophore corresponds to
the earliest stage in the evolution of placentotrophic incubation (incipient placentotrophy). Species with macrolecithal
oocytes (smaller than the brood cavity), a functionally active
embryophore and substantial embryonic increase could exemplify the next step, representing an intermediate stage in the
evolution of placentotrophy. My data show that such species in
Bryozoa exhibit the entire range of egg sizes from large (more
than 300 μm in Cribricellina cribraria ) to tiny (about 50 μm
in Beania bilaminata ) along with embryophore development,
thus demonstrating a decrease in the size of macrolecithal
oocytes, a corresponding decrease in ovarian activity and,
oppositely, an increase in placental activity. Thus, a shift from
incipient to substantial matrotrophy/placentotrophy occurred
in species with macrolecithal oogenesis. Until now, such
variation in maternal provisioning and placental structure has
been recorded only in squamate reptiles (Stewart 1992 ;
Blackburn 1993 , 1999a ; Stewart and Thompson 2000 ) and
3 Evolution of Reproductive Patterns in Cheilostomata
embryophore to one that was active, and thus from incipient
to substantial placentotrophy. The redistribution of the load
was refl ected in the structure of the ovary – fi rst of all, in the
number and size of its cells. Oocytes gradually became
smaller, accumulated less yolk and began to ripen faster.
A commonly accepted scenario for the evolution of
matrotrophy is based on the development of viviparous vertebrates (see Packard et al. 1977 ; Blackburn 1992 , 1993 ,
1999a , 2005a , 2006 ). In this case, internal fertilization and
retention of eggs are the major preconditions. Primitive fetal
nutrition would have been strictly lecithotrophic and developed further by the addition of small quantities of nutrients
from the reproductive tract of the viviparous female. This
so-called “incipient matrotrophy” is considered to have been
an initial step towards the evolution of the “specialized”
(Wourms 1981 ) or “substantial matrotrophy” (Blackburn
1992 ) that was accompanied by a subsequent shift in oogenesis. Examples corresponding to this scenario have been
thoroughly studied in squamate reptiles (reviewed in
Blackburn 1992 ) and poeciliid fi shes (Reznick et al. 2002 ;
Pollux et al. 2009 ; reviewed in Wourms 1981 ; MarshMatthews et al. 2010 ). When we deal with placenta-like systems, the term “incipient placentotrophy” can be applied
(Blackburn 1993 , 2005a , b ).
As for invertebrates, incipient matrotrophy (and sometimes placentotrophy) almost certainly exists among
onychophorans (Anderson 1973 ), scorpions (Farley 2001 )
and insects (Hagan 1951 ), although no defi nitive statements
concerning this phenomenon have been made.
My results indicate that both incipient and substantial
placentotrophy is present among cheilostome bryozoans.
Moreover, the fi nding of different modes of oogenesis and
degrees of embryonic enlargement and embryophore development in a variety of species (see Sects. 1.2.5 and 1.2.6 )
gives insight into the scenario(s) of transition from one of
these nutritional modes to the other. Considering cheilostomes with reproductive pattern IV fi rst, small placental
analogues (embryophores) have been recorded in four species with large macrolecithal oocytes that are slightly smaller
than the brood cavity or comparable in size to it ( Klugefl ustra
antarctica , Isosecurifl ustra angusta , Micropora notialis and
Figularia fi gularis ). Slight/negligible (ca 1.5-fold) enlargement of the embryo in them suggests a small nutrient supply.
Ultrastructural or experimental evidence is missing and it is
possible that EEN is absent. Hypertrophy and increase in the
number of embryophore cells together with the change in the
staining of their cytoplasm might then be explained, for
instance, by active gas exchange or/and removal of waste
material from the brood chamber. The most important sign
of a maternal-fetal physiological relationship is a recognizable response of the maternal cells to the appearance of a
zygote in the brood chamber, which points to molecular
transport. Even if EEN is absent, the establishment of such a
relationship can be the basis for further acquisition of
matrotrophy. In passing, it may be noted that mother-toembryo nutrient transfer has been recorded in experiments
involving a number of poeciliid teleost fi shes with large
yolky eggs (Marsh-Matthews et al. 2010 ).
In three species ( Cellaria tenuirostris , Cribricellina
cribraria and Watersipora subtorquata ) with the same reproductive pattern (IV), the embryo becomes noticeably larger
(3–3.39-fold increase) in comparison with mature macrolecithal eggs, despite hypertrophy of the embryophore cells
in these species being rather modest. Thus, a degree of morphological development of the placental analogue is not necessarily directly correlated with its nutritive activity.
Elaboration of placental structures has been known to correlate with a degree of nutritional provisioning during gestation in teleost fi shes (Turner 1940 ) and some scinks
(Flemming and Blackburn 2003 ), but my data show that it is
not always the case in cheilostomes (Ostrovsky 2013 ).
In six other cheilostomes (pattern IV, Beania bilaminata ,
Bicellariella ciliata , Celleporella hyalina , “ Calyptotheca ”
variolosa , Costaticella solida , C . bicuspis ), embryo enlargement is substantial or even very substantial and comparable
with that in species with pattern III [Despite the absence of
late embryos in available colonies C . bicuspis , a welldeveloped embryophore and the size difference between the
early embryo and the brood cavity allows for the inclusion of
this species here]. Actually, except for differences in mode of
oogenesis (macrolecithal vs oligolecithal), these two reproductive variations are identical, both involving an embryophore with strongly hypertrophied cells and eggs that are
considerably smaller than the brood cavity (Moosburgger
et al. 2012 ; Ostrovsky 2013 ).
Based on this information, it might be suggested that a
combination of large macrolecithal oocytes comparable in
size to that of the brood cavity, and minimal embryonic
enlargement provided by a small embryophore corresponds to
the earliest stage in the evolution of placentotrophic incubation (incipient placentotrophy). Species with macrolecithal
oocytes (smaller than the brood cavity), a functionally active
embryophore and substantial embryonic increase could exemplify the next step, representing an intermediate stage in the
evolution of placentotrophy. My data show that such species in
Bryozoa exhibit the entire range of egg sizes from large (more
than 300 μm in Cribricellina cribraria ) to tiny (about 50 μm
in Beania bilaminata ) along with embryophore development,
thus demonstrating a decrease in the size of macrolecithal
oocytes, a corresponding decrease in ovarian activity and,
oppositely, an increase in placental activity. Thus, a shift from
incipient to substantial matrotrophy/placentotrophy occurred
in species with macrolecithal oogenesis. Until now, such
variation in maternal provisioning and placental structure has
been recorded only in squamate reptiles (Stewart 1992 ;
Blackburn 1993 , 1999a ; Stewart and Thompson 2000 ) and
3 Evolution of Reproductive Patterns in Cheilostomata