13
2002b , 2009 ). Contrary to the above studies, Yund and
McCartney ( 1994 ) concluded from a fi eld experiment that C.
hyalina is able to use self-fertilization productively when
opportunity for outcrossing is limited. Yund and McCartney’s
experiment, however, could not exclude the possibility of
outcrossing through stored sperm (see below). Hughes and
Wright ( in press ) found that colonies from Yund and
McCartney’s population failed to produce embryos when
reared in strictly controlled reproductive isolation. The ability to reproduce through self-fertilization without incurring
inbreeding depression, however, appears to be universal
within the Celleporella angusta clade (Hughes et al. 2002b ;
Hughes and Wright, in press ).
Experiments conducted by Johnson ( 2010 ) showed selfi ng
in isolated colonies of Bugula stolonifera that produced viable larvae able to complete metamorphosis. Such colonies,
however, produced fewer larvae overall (comparing to crossfertilized colonies) and many were not able to initiate or complete metamorphosis. Colonies that formed from such larvae
in the fi eld also showed decreased survival and reproductive
fi tness. At present it is thought that intracolonial self-fertilization in bryozoans does occur but is only resorted to when
cross-fertilization is impossible (Hunter and Hughes 1993 ;
Yund and McCartney 1994 ; Hughes et al. 2002b ; reviewed in
Ostrovsky 2008b ; see also Johnson 2010 ). However, the ability of young Celleporella hyalina colonies, consisting of as
few as three zooids, to obtain and store sperm for up to
3–6 weeks (Hughes et al. 2002a ), casts doubts on the correctness of the cultivation methods used and hence on the results
of at least several earlier experiments in which isolated colonies reproduced successfully (Dyrynda and King 1982 ;
Maturo 1991a ; Temkin 1994 ). If sperm can be obtained by a
very young colony and can travel further to the sites of ovary
formation, then selfi ng ability is redundant.
1.2.2 Position of Gonads
It is assumed that the primordial germ cells (PGC) are probably formed from totipotent cells that in turn are the result of
dedifferentiation of mesothelial cells. The earliest sex cells
recognizable by light microscopy are considered to be spermatogonia and oogonia (Hayward 1983 ; Reed 1991 ).
Spermatogonia are formed within the cystid mesothelium
that lines the body cavity and/or within funicular strands.
First oogonia appear in or beneath the mesothelium of the
polypide bud or within the bilayered cystid lining in fully
formed zooids. Mature gonads (non-paired ovary and spermatogenic tissue) are located on the inner surface of the
cystid wall (being always associated with the funicular
cords) or on the cords themselves, sometimes close to the
polypide. Mature gametes fi rst enter the body cavity and then
are released into the environment via gonopores (Hageman
1983 ; Reed 1991 ; Woollacott 1999 ; Ostrovsky 2009 ).
1.2.2.1 Spermatogenic Tissue
The male gonad in bryozoans lacks any cell walls, ducts and
accessory glands. It was referred to as a testis or testes in
early works although the term spermatogenic tissue is more
appropriate because of its “loose” nature (see also Hughes
1987 ; Reed 1991 ). This tissue is either continuous or consists
of diffuse cell clusters (Figs. 1.34A, B and 1.18E ). Numerous
mitotic divisions of the primordial germ cells lead to the
formation of spermatogonia, which are associated with the
mesothelium of the body wall, funicular strands or both.
Some of them migrate into the cystid cavity. Spermatogonial
divisions result in morulae consisting of spermatocytes
united around the central cytoplasmic mass (cytophore)
(Figs. 1.18D and 1.34C ). Each spermatocyte undergoes meiotic division and four spermatids emerge. The latter undergo
a complex transformation (spermatogenesis) and become
spermatozoids. Mature spermatogenic tissue is a loose heterogeneous complex of male gametes and their progenitors
of different generations at different stages of the development
(Fig. 1.34B ) (reviewed by Franzén 1977 and Reed 1991 ).
The position of the male gonad differs in different species. According to Franzén ( 1977 ), Gymnolaemata have a
single testis located on the basal wall or on the funiculus,
usually in the proximal part of the cystid. Nevertheless,
paired testes were reported by Ehlers ( 1876 ), Braem ( 1896 )
and Silbermann ( 1906 ) (in the ctenostomes Hypophorella
expansa , Paludicella articulata and Alcyonidium mytili ) and
by Vigelius ( 1884b ) (in the cheilostome Chartella membranaceotruncata ). In Membranipora serrilamella , diffuse
groups of spermatogonia were found on basal and lateral
zooidal walls at the earliest stages of zooid maturation [lacking a functional polypide] (Hageman 1983 ; Reed 1991 ). As
reported in the literature, spermatogenic tissue develops only
in the proximal part of the zooid in 20 cheilostome species
and in both proximal and distal parts in 17 cheilostome species. A solely distal position for the male gonad was recorded
in only one cheilostome species Cellaria fi stulosa (Calvet
1900 ; Ostrovsky et al. 2008 ; see also Appendix I).
My own anatomical data agree very well with the above
fi ndings. As a rule, the male gonad is a single structure but in
nine species two loci of formation of male gametes were
found, one in the proximal part of the zooid and the other
distal. For example, in Hippoporina reticulatopunctata
spermatogenic tissue is located in the corner between the
proximal transverse wall and the frontal wall, while in the
distal part of the zooid it is located on the lateral walls. In 32
species spermatogenic tissue was noted only in the proximal
half of the zooid, in eight species only in the distal part, and
in 22 species both in the distal and proximal parts of the
zooid (either as two isolated loci or as an uninterrupted cell
mass on the cystid basal wall) (see Table 1.2 ).
Altogether I found about 20 variants of spermatogenic
tissue location, differing as to its position on the zooidal wall
and/or funicular cords. In most cheilostomes studied, the male
1.2 Reproductive Patterns of Bryozoa
2002b , 2009 ). Contrary to the above studies, Yund and
McCartney ( 1994 ) concluded from a fi eld experiment that C.
hyalina is able to use self-fertilization productively when
opportunity for outcrossing is limited. Yund and McCartney’s
experiment, however, could not exclude the possibility of
outcrossing through stored sperm (see below). Hughes and
Wright ( in press ) found that colonies from Yund and
McCartney’s population failed to produce embryos when
reared in strictly controlled reproductive isolation. The ability to reproduce through self-fertilization without incurring
inbreeding depression, however, appears to be universal
within the Celleporella angusta clade (Hughes et al. 2002b ;
Hughes and Wright, in press ).
Experiments conducted by Johnson ( 2010 ) showed selfi ng
in isolated colonies of Bugula stolonifera that produced viable larvae able to complete metamorphosis. Such colonies,
however, produced fewer larvae overall (comparing to crossfertilized colonies) and many were not able to initiate or complete metamorphosis. Colonies that formed from such larvae
in the fi eld also showed decreased survival and reproductive
fi tness. At present it is thought that intracolonial self-fertilization in bryozoans does occur but is only resorted to when
cross-fertilization is impossible (Hunter and Hughes 1993 ;
Yund and McCartney 1994 ; Hughes et al. 2002b ; reviewed in
Ostrovsky 2008b ; see also Johnson 2010 ). However, the ability of young Celleporella hyalina colonies, consisting of as
few as three zooids, to obtain and store sperm for up to
3–6 weeks (Hughes et al. 2002a ), casts doubts on the correctness of the cultivation methods used and hence on the results
of at least several earlier experiments in which isolated colonies reproduced successfully (Dyrynda and King 1982 ;
Maturo 1991a ; Temkin 1994 ). If sperm can be obtained by a
very young colony and can travel further to the sites of ovary
formation, then selfi ng ability is redundant.
1.2.2 Position of Gonads
It is assumed that the primordial germ cells (PGC) are probably formed from totipotent cells that in turn are the result of
dedifferentiation of mesothelial cells. The earliest sex cells
recognizable by light microscopy are considered to be spermatogonia and oogonia (Hayward 1983 ; Reed 1991 ).
Spermatogonia are formed within the cystid mesothelium
that lines the body cavity and/or within funicular strands.
First oogonia appear in or beneath the mesothelium of the
polypide bud or within the bilayered cystid lining in fully
formed zooids. Mature gonads (non-paired ovary and spermatogenic tissue) are located on the inner surface of the
cystid wall (being always associated with the funicular
cords) or on the cords themselves, sometimes close to the
polypide. Mature gametes fi rst enter the body cavity and then
are released into the environment via gonopores (Hageman
1983 ; Reed 1991 ; Woollacott 1999 ; Ostrovsky 2009 ).
1.2.2.1 Spermatogenic Tissue
The male gonad in bryozoans lacks any cell walls, ducts and
accessory glands. It was referred to as a testis or testes in
early works although the term spermatogenic tissue is more
appropriate because of its “loose” nature (see also Hughes
1987 ; Reed 1991 ). This tissue is either continuous or consists
of diffuse cell clusters (Figs. 1.34A, B and 1.18E ). Numerous
mitotic divisions of the primordial germ cells lead to the
formation of spermatogonia, which are associated with the
mesothelium of the body wall, funicular strands or both.
Some of them migrate into the cystid cavity. Spermatogonial
divisions result in morulae consisting of spermatocytes
united around the central cytoplasmic mass (cytophore)
(Figs. 1.18D and 1.34C ). Each spermatocyte undergoes meiotic division and four spermatids emerge. The latter undergo
a complex transformation (spermatogenesis) and become
spermatozoids. Mature spermatogenic tissue is a loose heterogeneous complex of male gametes and their progenitors
of different generations at different stages of the development
(Fig. 1.34B ) (reviewed by Franzén 1977 and Reed 1991 ).
The position of the male gonad differs in different species. According to Franzén ( 1977 ), Gymnolaemata have a
single testis located on the basal wall or on the funiculus,
usually in the proximal part of the cystid. Nevertheless,
paired testes were reported by Ehlers ( 1876 ), Braem ( 1896 )
and Silbermann ( 1906 ) (in the ctenostomes Hypophorella
expansa , Paludicella articulata and Alcyonidium mytili ) and
by Vigelius ( 1884b ) (in the cheilostome Chartella membranaceotruncata ). In Membranipora serrilamella , diffuse
groups of spermatogonia were found on basal and lateral
zooidal walls at the earliest stages of zooid maturation [lacking a functional polypide] (Hageman 1983 ; Reed 1991 ). As
reported in the literature, spermatogenic tissue develops only
in the proximal part of the zooid in 20 cheilostome species
and in both proximal and distal parts in 17 cheilostome species. A solely distal position for the male gonad was recorded
in only one cheilostome species Cellaria fi stulosa (Calvet
1900 ; Ostrovsky et al. 2008 ; see also Appendix I).
My own anatomical data agree very well with the above
fi ndings. As a rule, the male gonad is a single structure but in
nine species two loci of formation of male gametes were
found, one in the proximal part of the zooid and the other
distal. For example, in Hippoporina reticulatopunctata
spermatogenic tissue is located in the corner between the
proximal transverse wall and the frontal wall, while in the
distal part of the zooid it is located on the lateral walls. In 32
species spermatogenic tissue was noted only in the proximal
half of the zooid, in eight species only in the distal part, and
in 22 species both in the distal and proximal parts of the
zooid (either as two isolated loci or as an uninterrupted cell
mass on the cystid basal wall) (see Table 1.2 ).
Altogether I found about 20 variants of spermatogenic
tissue location, differing as to its position on the zooidal wall
and/or funicular cords. In most cheilostomes studied, the male
1.2 Reproductive Patterns of Bryozoa