263
may belong to the same superfamily, has evolved matrotrophic incubation (reproductive pattern IV).
Broadcasting in Victorella pavida and V . pseudoarachnidia (see Braem 1951 ; Jebram and Everitt 1982 ) (although
the actual larvae are unknown), lecithotrophy and various
modes of parental care including extraembryonic nutrition
(that is, reproductive patterns I, II and III) have been
recorded in the superfamily Victorelloidea. The evolution of
brooding in this group proceeded from attachment of
oocytes to the cystid ( Pottsiella erecta ) to their immersion in
the cystid wall ( Tanganella appendiculata , Panolicella
nutans ) and, on this basis, the origin of matrotrophy ( Nolella ,
Sundanella ) as well as temporary ( Bulbella abscondita ) or
“permanent” ( Immergentia suecica , Spathipora comma , T .
muelleri ) retraction of embryos into the introvert. In the latter species the embryos are also immersed in the vestibulum
wall. Also, the lecithotrophic larva of B . abscondita has a
rudimentary gut.
Cyphonautes larvae ( Farrella repens , Hypopharella
expansa ) and coronate larvae, external ( Triticella fl ava ) and
internal (in the introvert) brooding as well as extraembryonic
nutrition ( Walkeria uva , Bantariella cookae ) have been
described in the superfamily Walkerioidea. This means that
this ctenostome group, too, is characterized by reproductive
patterns I, II and III.
In all species of the superfamily Vesicularioidea, embryos
develop in the introvert, but the phylogenetic position of this
group indicates that their ancestry featured a planktotrophic
larva. The only mode of brooding in this superfamily is in the
introvert, and Zoobotryon verticillatum has extraembryonic
nutrition. Hence, this superfamily possesses reproductive
patterns II and III.
A comparison of the reproductive variants among the
ctenostome clades shows that the evolution of brooding in
each of them followed a similar or the same scenario – from
external to internal brooding in an invagination of the body
wall and/or introvert. The occurrence of planktotrophy and
lecithotrophy within the same groups indicates multiple independent origins of non-feeding larvae within Alcyonidioidea,
Walkerioidea, Victorelloidea and Vesicularioidea. As in the
Cheilostomata, lecithotrophy always accompanies brooding,
which may point to a connection between these two phenomena. It is quite possible that the endotrophic larva evolved in
ctenostomes as often, and approximately at the same time, as
brooding did. The simplest mode of external brooding is
found in the freshwater ctenostome Paludicella articulata
(superfamily Paludicelloidea). Judging from the position of
Paludicelloidea in the phylogenetic tree of ctenostomes,
brooding evolved independently in this group also.
The above comparative analysis of reproductive patterns
in ctenostome bryozoans illustrates one possible trend in the
evolution of oogenesis in this order – a reduction in the number of oocytes produced or maturing in a zooid. Although the
total number of female gametes forming in the ovary of most
ctenostomes is still rather considerable, relatively few of
them mature and are brooded. An apparent trend towards
oocyte enlargement is also indicated but it is not so well
expressed as in cheilostomes. Additionally, as in cheilostomes, brooding may compensate for the decrease in the
number of maturing eggs in ctenostomes. In general, these
evolutionary pathways are accompanied by a shift to lecithotrophy strongly reminiscent of the scenarios suggested
for Cheilostomata.
Another important aspect of ctenostome evolution is the
independent origin of matrotrophy in different clades (superfamilies). Embryonic enlargement is recorded within the
Alcyonidioidea,
Walkerioidea,
Victorelloidea
and
Vesicularioidea, as well as in Labiostomella gisleni . The
immersion of eggs in the zooid wall or their transfer to the
introvert for incubation, thereby isolating the brood cavity
from the external medium and also allowing physiological
exchange between the oocyte and the cystid wall, may have
promoted the evolution of the embryophore in some ctenostomes. The available data indicate that extraembryonic
nutrition evolved in ctenostomes at least fi ve times.
3.4.4.3 Parallel Evolution of Reproductive
Patterns in Ctenostomata and
Cheilostomata
Summing up the above comparisons, the reproductive patterns in the Ctenostomata are similar or identical to those in
the Cheilostomata (the only exception being viviparity,
which is unknown among ctenostomes). The evolution of
sexual reproduction in these two orders as well as in different
ctenostome superfamilies shows similar trends, with many
novelties originating more than once, independently and at
different times. Distinct parallels observed in ctenostomes
and cheilostomes may be connected to the phylogenetic
relatedness of these two groups, the Ctenostomata being
paraphyletic with respect to Cheilostomata. Actually, the
same general trends are characteristic of all Bryozoa, and a
change in one character (the acquisition of a novelty) triggered a similar cascade of morphogenetic events, although
these transformations sometimes involved different structures. Increasing oocyte size (accompanied by a decrease in
their number) was the basis for the evolution of lecithotrophy. The origin of a non-feeding larva in bryozoans must
have been somehow associated with the origin of embryonic
incubation, with different structures being involved in the
formation of brood chambers (spines, kenozooids, body-wall
invaginations and evaginations). Further, parental care
changed from external brooding towards the more reliable
internal mode. In its turn, internal incubation (brooding or
viviparity) was a prerequisite for the origin of extraembryonic nutrition, with matrotrophic structures being evolved
on the basis of ovaries (Cyclostomata, Cheilostomata), a
3.4 Causes, Stages and Consequences of Transition to Endotrophy in Cheilostomata and Ctenostomata
may belong to the same superfamily, has evolved matrotrophic incubation (reproductive pattern IV).
Broadcasting in Victorella pavida and V . pseudoarachnidia (see Braem 1951 ; Jebram and Everitt 1982 ) (although
the actual larvae are unknown), lecithotrophy and various
modes of parental care including extraembryonic nutrition
(that is, reproductive patterns I, II and III) have been
recorded in the superfamily Victorelloidea. The evolution of
brooding in this group proceeded from attachment of
oocytes to the cystid ( Pottsiella erecta ) to their immersion in
the cystid wall ( Tanganella appendiculata , Panolicella
nutans ) and, on this basis, the origin of matrotrophy ( Nolella ,
Sundanella ) as well as temporary ( Bulbella abscondita ) or
“permanent” ( Immergentia suecica , Spathipora comma , T .
muelleri ) retraction of embryos into the introvert. In the latter species the embryos are also immersed in the vestibulum
wall. Also, the lecithotrophic larva of B . abscondita has a
rudimentary gut.
Cyphonautes larvae ( Farrella repens , Hypopharella
expansa ) and coronate larvae, external ( Triticella fl ava ) and
internal (in the introvert) brooding as well as extraembryonic
nutrition ( Walkeria uva , Bantariella cookae ) have been
described in the superfamily Walkerioidea. This means that
this ctenostome group, too, is characterized by reproductive
patterns I, II and III.
In all species of the superfamily Vesicularioidea, embryos
develop in the introvert, but the phylogenetic position of this
group indicates that their ancestry featured a planktotrophic
larva. The only mode of brooding in this superfamily is in the
introvert, and Zoobotryon verticillatum has extraembryonic
nutrition. Hence, this superfamily possesses reproductive
patterns II and III.
A comparison of the reproductive variants among the
ctenostome clades shows that the evolution of brooding in
each of them followed a similar or the same scenario – from
external to internal brooding in an invagination of the body
wall and/or introvert. The occurrence of planktotrophy and
lecithotrophy within the same groups indicates multiple independent origins of non-feeding larvae within Alcyonidioidea,
Walkerioidea, Victorelloidea and Vesicularioidea. As in the
Cheilostomata, lecithotrophy always accompanies brooding,
which may point to a connection between these two phenomena. It is quite possible that the endotrophic larva evolved in
ctenostomes as often, and approximately at the same time, as
brooding did. The simplest mode of external brooding is
found in the freshwater ctenostome Paludicella articulata
(superfamily Paludicelloidea). Judging from the position of
Paludicelloidea in the phylogenetic tree of ctenostomes,
brooding evolved independently in this group also.
The above comparative analysis of reproductive patterns
in ctenostome bryozoans illustrates one possible trend in the
evolution of oogenesis in this order – a reduction in the number of oocytes produced or maturing in a zooid. Although the
total number of female gametes forming in the ovary of most
ctenostomes is still rather considerable, relatively few of
them mature and are brooded. An apparent trend towards
oocyte enlargement is also indicated but it is not so well
expressed as in cheilostomes. Additionally, as in cheilostomes, brooding may compensate for the decrease in the
number of maturing eggs in ctenostomes. In general, these
evolutionary pathways are accompanied by a shift to lecithotrophy strongly reminiscent of the scenarios suggested
for Cheilostomata.
Another important aspect of ctenostome evolution is the
independent origin of matrotrophy in different clades (superfamilies). Embryonic enlargement is recorded within the
Alcyonidioidea,
Walkerioidea,
Victorelloidea
and
Vesicularioidea, as well as in Labiostomella gisleni . The
immersion of eggs in the zooid wall or their transfer to the
introvert for incubation, thereby isolating the brood cavity
from the external medium and also allowing physiological
exchange between the oocyte and the cystid wall, may have
promoted the evolution of the embryophore in some ctenostomes. The available data indicate that extraembryonic
nutrition evolved in ctenostomes at least fi ve times.
3.4.4.3 Parallel Evolution of Reproductive
Patterns in Ctenostomata and
Cheilostomata
Summing up the above comparisons, the reproductive patterns in the Ctenostomata are similar or identical to those in
the Cheilostomata (the only exception being viviparity,
which is unknown among ctenostomes). The evolution of
sexual reproduction in these two orders as well as in different
ctenostome superfamilies shows similar trends, with many
novelties originating more than once, independently and at
different times. Distinct parallels observed in ctenostomes
and cheilostomes may be connected to the phylogenetic
relatedness of these two groups, the Ctenostomata being
paraphyletic with respect to Cheilostomata. Actually, the
same general trends are characteristic of all Bryozoa, and a
change in one character (the acquisition of a novelty) triggered a similar cascade of morphogenetic events, although
these transformations sometimes involved different structures. Increasing oocyte size (accompanied by a decrease in
their number) was the basis for the evolution of lecithotrophy. The origin of a non-feeding larva in bryozoans must
have been somehow associated with the origin of embryonic
incubation, with different structures being involved in the
formation of brood chambers (spines, kenozooids, body-wall
invaginations and evaginations). Further, parental care
changed from external brooding towards the more reliable
internal mode. In its turn, internal incubation (brooding or
viviparity) was a prerequisite for the origin of extraembryonic nutrition, with matrotrophic structures being evolved
on the basis of ovaries (Cyclostomata, Cheilostomata), a
3.4 Causes, Stages and Consequences of Transition to Endotrophy in Cheilostomata and Ctenostomata