244
of bryozoans, possibly increasing the probability of contact
between male and female gametes.
The type of reproduction when only sperm is released into
the environment and enters female individuals or zooids is
referred to as spermcast mating (Bishop and Pemberton
2006 ). In spite of the apparent very high risk of sperm mortality, fertilization success in gymnolaemate bryozoans is very
high too, varying from 83 to 100% (Temkin 1994 , 1996 ; Yund
and McCartney 1994 ; Bishop and Pemberton 2006 ).
Moreover, all of the bryozoans studied, including stenolaemates and phylactolaemates, have intraovarian fertilization.
In the broadcasters studied (two malacostegines and a ctenostome), fertilization occurs immediately before or during
ovulation (Temkin 1994 , 1996 ). In the brooding ctenostome
Boverbankia gracilis , sperm penetrates the mature macrolecithal oocyte located in the ovary (Temkin 1996 ), whereas in
Nolella stipata and Alcyonidium sp. sperm was found in the
ovary in “growing” oocytes (developmental stage not indicated) (Marcus 1938 ). Thus, it seems that in brooding ctenostomes fertilization occurs in the ovary, apparently at a rather
late stage of oocyte development. In contrast, Chrétien ( 1958 )
wrote that in A . diaphanum polypide degeneration begins
before vitellogenesis starts, i.e. the alien sperm should be
obtained by a zooid during much earlier stages of the oogenesis. Similarly, in all the brooding cheilostomes studied, early
oocytes are fertilized (see Sect. 1.3.6 ).
So, one may suggest that the evolution of fertilization in
Gymnolaemata proceeded towards earlier fusion of male and
female gametes. “Ovulatory” fertilization (during ovulation
or immediately after it) became intraovarian (Ostrovsky
2008 , 2009 ). This shift may be perceived to enhance sperm
survival – spermatozoids probably could live longer by
entering the ovary. Moreover, in this instance of sperm storage the zooid, having once obtained sperm, no longer
depends on an additional fertilization event.
Why or how cheilostomes acquired very early (precocious) fertilization of early primary oocytes is unclear (see
Sect. 1.3.6 ). It may have been a side effect of the evolution
of internal fertilization itself, ensuring the meeting of gametes in small immobile epibionts. Sperm succeeding in
entering the ovary began to fuse with very young oocytes.
Important consequences of early fertilization would have
been (1) the development of oocytes in pairs (oocyte doublets)
and (2) dependence of the inception of vitellogenesis upon
fertilization.
In Membranipora membranacea , the division of the
oogonium results in a pair of early primary oocytes that
remain connected by a cytoplasmic bridge for some time
(Hageman 1983 ). If the earliest brooding cheilostomes had
had the same feature, then the transition to precocious intraovarian fertilization and fusion of one of two young oocytes
(still connected by a cytoplasmic bridge) with the male gamete could have prevented the completion of cytokinesis.
Syngamy typically triggers a cortical reaction that transforms a vitelline membrane into a fertilization envelope. In
the case of an oocyte doublet, such an envelope should form
around both cells since their membranes are still continuous
(Ostrovsky 2008 ). Detachment of the fertilization envelope
from the oolemma is delayed, however, and this may prevent
young oocytes from completing cytokinesis. Thus, siblings
are forced to stay together, further differentiating into the
vitellogenic oocyte and its nurse cell. A detailed ultrastructural study of early oocyte doublets would shed light on this
problem. For instance, Dyrynda and King ( 1983 , p. 475)
recorded what they called “the precursor of the vitelline
envelope” or “primary coat” around both the oocyte and its
nurse cell during early vitellogenesis in two cheilostome
brooders. Further evidence in support of the idea that nurse
cells originated as a result of early fertilization is their
absence in broadcasting cheilostomes and brooding ctenostomes, which appear to lack early fertilization (but see
example of A . diaphanum in Chrétien 1958 ).
A rather curious observation was made by Marcus ( 1941a )
who wrote that in Thalamoporella evelinae the nurse cell fi rst
fuses with the oocyte and then fertilization occurs. This information should be verifi ed but if it is true it means that reproductive pattern II emerged in Thalamoporella independently,
as did its ovicells. Marcus ( 1934 ) also described and illustrated what he called “nurse cells” in the phylactolaemate
Lophopus crystallinus . He considered them abortive oocytes
but in his illustrations the cell pairs consisting of an oocyte
and a “nurse cell” closely resemble oocyte doublets in cheilostomes. It is unfortunately not known if these cells are real
siblings or if there is a cytoplasmic bridge between them.
The presence of nurse cells in the viviparous Epistomiidae
remains unclear. If the so-called “follicle” cells surrounding
the oocyte (Dyrynda and King 1982 ) are not nurse cells but
cells of the ovary wall, then nurse cells could have been lost
in this family, and the single oocyte is formed from a single
oogonium. If the “follicle” is of germ-cell origin then the
nurse cells substitute an ovary. Gordon ( 2012 ) placed
Epistomiidae near Beaniidae in his classifi cation, and incubation in the latter family occurs in internal brood sacs. If
epistomiids are indeed related to beaniids, they may have
lost brood chambers when they became viviparous.
Specialization of the nurse cells in Cheilostomata was
related to the change in their synthesizing activity. Yolk
granules in the cytoplasm of the nurse cells have been found
in about 30 bryozoan species (see Table 1.7 ). Their presence
may indicate that in the early stages of evolution of the new
reproductive pattern nurse cells functioned identically to
oocytes, forming a nutrient reserve (yolk), but it is unclear if
this reserve was transported to the sibling. Later, nurse cells
in most species began to produce mostly RNA, presumably
transporting it to the sibling’s cytoplasm across the cytoplasmic bridge (see Dyrynda and King 1983 ). Hypertrophied
3 Evolution of Reproductive Patterns in Cheilostomata
of bryozoans, possibly increasing the probability of contact
between male and female gametes.
The type of reproduction when only sperm is released into
the environment and enters female individuals or zooids is
referred to as spermcast mating (Bishop and Pemberton
2006 ). In spite of the apparent very high risk of sperm mortality, fertilization success in gymnolaemate bryozoans is very
high too, varying from 83 to 100% (Temkin 1994 , 1996 ; Yund
and McCartney 1994 ; Bishop and Pemberton 2006 ).
Moreover, all of the bryozoans studied, including stenolaemates and phylactolaemates, have intraovarian fertilization.
In the broadcasters studied (two malacostegines and a ctenostome), fertilization occurs immediately before or during
ovulation (Temkin 1994 , 1996 ). In the brooding ctenostome
Boverbankia gracilis , sperm penetrates the mature macrolecithal oocyte located in the ovary (Temkin 1996 ), whereas in
Nolella stipata and Alcyonidium sp. sperm was found in the
ovary in “growing” oocytes (developmental stage not indicated) (Marcus 1938 ). Thus, it seems that in brooding ctenostomes fertilization occurs in the ovary, apparently at a rather
late stage of oocyte development. In contrast, Chrétien ( 1958 )
wrote that in A . diaphanum polypide degeneration begins
before vitellogenesis starts, i.e. the alien sperm should be
obtained by a zooid during much earlier stages of the oogenesis. Similarly, in all the brooding cheilostomes studied, early
oocytes are fertilized (see Sect. 1.3.6 ).
So, one may suggest that the evolution of fertilization in
Gymnolaemata proceeded towards earlier fusion of male and
female gametes. “Ovulatory” fertilization (during ovulation
or immediately after it) became intraovarian (Ostrovsky
2008 , 2009 ). This shift may be perceived to enhance sperm
survival – spermatozoids probably could live longer by
entering the ovary. Moreover, in this instance of sperm storage the zooid, having once obtained sperm, no longer
depends on an additional fertilization event.
Why or how cheilostomes acquired very early (precocious) fertilization of early primary oocytes is unclear (see
Sect. 1.3.6 ). It may have been a side effect of the evolution
of internal fertilization itself, ensuring the meeting of gametes in small immobile epibionts. Sperm succeeding in
entering the ovary began to fuse with very young oocytes.
Important consequences of early fertilization would have
been (1) the development of oocytes in pairs (oocyte doublets)
and (2) dependence of the inception of vitellogenesis upon
fertilization.
In Membranipora membranacea , the division of the
oogonium results in a pair of early primary oocytes that
remain connected by a cytoplasmic bridge for some time
(Hageman 1983 ). If the earliest brooding cheilostomes had
had the same feature, then the transition to precocious intraovarian fertilization and fusion of one of two young oocytes
(still connected by a cytoplasmic bridge) with the male gamete could have prevented the completion of cytokinesis.
Syngamy typically triggers a cortical reaction that transforms a vitelline membrane into a fertilization envelope. In
the case of an oocyte doublet, such an envelope should form
around both cells since their membranes are still continuous
(Ostrovsky 2008 ). Detachment of the fertilization envelope
from the oolemma is delayed, however, and this may prevent
young oocytes from completing cytokinesis. Thus, siblings
are forced to stay together, further differentiating into the
vitellogenic oocyte and its nurse cell. A detailed ultrastructural study of early oocyte doublets would shed light on this
problem. For instance, Dyrynda and King ( 1983 , p. 475)
recorded what they called “the precursor of the vitelline
envelope” or “primary coat” around both the oocyte and its
nurse cell during early vitellogenesis in two cheilostome
brooders. Further evidence in support of the idea that nurse
cells originated as a result of early fertilization is their
absence in broadcasting cheilostomes and brooding ctenostomes, which appear to lack early fertilization (but see
example of A . diaphanum in Chrétien 1958 ).
A rather curious observation was made by Marcus ( 1941a )
who wrote that in Thalamoporella evelinae the nurse cell fi rst
fuses with the oocyte and then fertilization occurs. This information should be verifi ed but if it is true it means that reproductive pattern II emerged in Thalamoporella independently,
as did its ovicells. Marcus ( 1934 ) also described and illustrated what he called “nurse cells” in the phylactolaemate
Lophopus crystallinus . He considered them abortive oocytes
but in his illustrations the cell pairs consisting of an oocyte
and a “nurse cell” closely resemble oocyte doublets in cheilostomes. It is unfortunately not known if these cells are real
siblings or if there is a cytoplasmic bridge between them.
The presence of nurse cells in the viviparous Epistomiidae
remains unclear. If the so-called “follicle” cells surrounding
the oocyte (Dyrynda and King 1982 ) are not nurse cells but
cells of the ovary wall, then nurse cells could have been lost
in this family, and the single oocyte is formed from a single
oogonium. If the “follicle” is of germ-cell origin then the
nurse cells substitute an ovary. Gordon ( 2012 ) placed
Epistomiidae near Beaniidae in his classifi cation, and incubation in the latter family occurs in internal brood sacs. If
epistomiids are indeed related to beaniids, they may have
lost brood chambers when they became viviparous.
Specialization of the nurse cells in Cheilostomata was
related to the change in their synthesizing activity. Yolk
granules in the cytoplasm of the nurse cells have been found
in about 30 bryozoan species (see Table 1.7 ). Their presence
may indicate that in the early stages of evolution of the new
reproductive pattern nurse cells functioned identically to
oocytes, forming a nutrient reserve (yolk), but it is unclear if
this reserve was transported to the sibling. Later, nurse cells
in most species began to produce mostly RNA, presumably
transporting it to the sibling’s cytoplasm across the cytoplasmic bridge (see Dyrynda and King 1983 ). Hypertrophied
3 Evolution of Reproductive Patterns in Cheilostomata