272
but body-wall outfolds. Ovicells with complete ooecia
originated by means of reduction in the number of spines
and their fl attening, the development of a proximally concave spine arrangement, the loss of articulation of spines
from the gymnocyst, and the fusion of spines. Further modifi cation of ovicells was closely connected with the evolution
of complex frontal shields. Reconstruction of the stages of
ovicell evolution provides further evidence for polyphyly of
lepraliomorph cheilostomes.
The main trends in the evolution of brooding structures in
the Cheilostomata were: (1) integration of zooids forming
the ovicell, (2) reduced ectooecial calcifi cation, (3) reduction
of the distal ooecium-producing zooid, (4) immersion of the
brood cavity with reduction of the ooecium and, as a consequence, the origin of internal brood sacs, (5) a change in the
method of ovicell closure, and (6) the origin of peristomial
ovicells. In many cheilostome families these changes were
independent.
Cheilostome evolution was accompanied by progressive
increases in colonial integration, one of the key factors in the
success of the order. Integration was expressed as corresponding changes in the sexual structure of the colony, in
synchronous maturation and spawning of gametes, sexual
zooidal polymorphism, and brooding in morphofunctional
modules (including ovicells). Sexual polymorphs and varied
sex-related structures in the colony were acquired repeatedly
in different cheilostome groups.
Importantly, the evolution of sexual reproduction in
Cheilostomata and Ctenostomata had similar trends, and
instances of parallelism abound. Viviparity evolved independently in the order Cyclostomata (class Stenolaemata) and
the family Epistomiidae (order Cheilostomata).
In the Mesozoic and the Tertiary cheilostome evolution was
accompanied by the appearance of novelties facilitating or
enhancing responses to environmental change. The highest
plasticity, expressed in the acquisition of effective means of
protection (spines, brood chambers, zooidal polymorphs, frontal shields), various growth forms and constructions of colonies, new reproductive patterns and larval types, as well as high
colonial integration and modular complexity, allowed cheilostomes to compete successfully with other epibionts, making
this order one of the most successful groups of colonial invertebrates. Generally, many of these novelties independently
evolved in other bryozoan clades as well, helping bryozoans to
survive mass extinctions and to remain a dominant group in
most benthic assemblages for over 450 million years.
References
Adiyodi KG, Adiyodi RG (eds) (1989) Reproductive biology of invertebrates, vol 4, Part A: fertilization, development, and parental
care. IBH Publishing Co Pvt Ltd, New Delhi/Bombay/Calcutta/
Oxford
Adiyodi KG, Adiyodi RG (eds) (1990) Reproductive biology of invertebrates, vol 4, Part B: fertilization, development, and parental care.
IBH Publishing Co Pvt Ltd, New Delhi/Bombay/Calcutta/Oxford
Adiyodi RG, Subramoniam T (1983) Arthropoda – Crustacea. In:
Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, vol 1, Oogenesis, oviposition, and oosorption. John Wiley
and Sons, Chichester, pp 443–495
Alatalo P, Berg J, Carl J, D’Asaro CN (1984) Reproduction and development in the lucinid clam Codakia orbicularis (Linne, 1758). Bull
Mar Sci 34(3):424–434
Allen JD, Pernet B (2007) Intermediate modes of larval development:
bridging the gap between planktotrophy and lecithotrophy. Evol
Dev 9(6):643–653
Allman G (1856) A monograph of the fresh-water Polyzoa, including
all the known species, both British and foreign. Ray Society, London
Anderson DT (1973) Embryology and phylogeny in annelids and
arthropods. Pergamon Press, New York
Arias A, Reznick D (2000) Life history of Phalloceros caudimaculatus :
a novel variation on the theme of lifebearing in the family
Poeciliidae. Copeia 2000(3):792–798
Atkins D (1955) The cyphonautes larvae of the Plymouth area and the
metamorphosis of Membranipora membranacea (L.). J Mar Biol
Assoc UK 34:441–449
Balon EK (1991) Probable evolution of the coelacanth’s reproductive
style: lecithotrophy and orally feeding embryos in cichlid fi shes and
in Latimeria chalumnae . Environ Biol Fish 32:249–265
Bancroft AJ (1986) Ovicells in Palaeozoic bryozoan order Fenestrata.
Palaeontology 29(1):155–164
Banta WC (1967) A new species of Victorella from Southern California
(Bryozoa, Ctenostomata). Proc US Natl Mus 122(3593):1–18
Banta WC (1968) Mimosella cookae , new species (Bryozoa,
Ctenostomata) with a review of the family Mimosellidae. Bull
South Calif Acad Sci 67:245–254
Barrera E, Savin SM (1999) Evolution of the Late CampanianMaastrichtian marine climates and oceans. In: Barrera E, Johnston
CC (eds) Evolution of the Cretaceous ocean-climate system.
Geological Society of America, Boulder, pp 245–282
Barrois J (1877) Recherches sur l’embryologie des bryozoaires. Trav St
Zool Wimereux 1:1–305
Batygina TB, Bragina EA, Ereskovsky AV, Ostrovsky AN (2006)
Viviparity in plants and animals: invertebrates and lower chordates.
Unipress, St Petersburg State University, St Petersburg [in Russian
with English summary]
Bermingham J, Wilkinson TL (2009) Embryo nutrition in parthenogenetic viviparous aphids. Physiol Entomol 34:103–109
Bishop JDD, Pemberton AJ (2006) The third way: spermcast mating in
sessile marine invertebrates. Integr Comp Biol 46:398–406
Bishop JDD, Manríquez PH, Hughes RN (2000) Water-borne sperm
trigger vitellogenic egg growth in two sessile marine invertebrates.
Proc R Soc B 267:1165–1169
Blackburn DG (1992) Convergent evolution of viviparity, matrotrophy,
and specializations for fetal nutrition in reptiles and other vertebrates. Am Zool 32(2):313–321
Blackburn DG (1993) Chorioallantoic placentation in squamate reptiles
– structure, function, development and evolution. J Exp Zool
266:414–430
Blackburn DG (1994) Standardized criteria for the recognition of
embryonic nutritional patterns in squamate reptiles. Copeia
4:925–935
Blackburn DG (1999a) Viviparity and oviparity: evolution and reproductive strategies. In: Knobil E, Neill JD (eds) Encyclopedia of
reproduction. Academic Press, New York, pp 994–1003
Blackburn DG (1999b) Placenta and placental analogs in reptiles and
amphibians. In: Knobil E, Neill JD (eds) Encyclopedia of reproduction. Academic Press, New York, pp 840–847
Blackburn DG (1999c) Are viviparity and egg-guarding evolutionarily
labile in squamates? Herpetologica 55:556–572
3 Evolution of Reproductive Patterns in Cheilostomata
but body-wall outfolds. Ovicells with complete ooecia
originated by means of reduction in the number of spines
and their fl attening, the development of a proximally concave spine arrangement, the loss of articulation of spines
from the gymnocyst, and the fusion of spines. Further modifi cation of ovicells was closely connected with the evolution
of complex frontal shields. Reconstruction of the stages of
ovicell evolution provides further evidence for polyphyly of
lepraliomorph cheilostomes.
The main trends in the evolution of brooding structures in
the Cheilostomata were: (1) integration of zooids forming
the ovicell, (2) reduced ectooecial calcifi cation, (3) reduction
of the distal ooecium-producing zooid, (4) immersion of the
brood cavity with reduction of the ooecium and, as a consequence, the origin of internal brood sacs, (5) a change in the
method of ovicell closure, and (6) the origin of peristomial
ovicells. In many cheilostome families these changes were
independent.
Cheilostome evolution was accompanied by progressive
increases in colonial integration, one of the key factors in the
success of the order. Integration was expressed as corresponding changes in the sexual structure of the colony, in
synchronous maturation and spawning of gametes, sexual
zooidal polymorphism, and brooding in morphofunctional
modules (including ovicells). Sexual polymorphs and varied
sex-related structures in the colony were acquired repeatedly
in different cheilostome groups.
Importantly, the evolution of sexual reproduction in
Cheilostomata and Ctenostomata had similar trends, and
instances of parallelism abound. Viviparity evolved independently in the order Cyclostomata (class Stenolaemata) and
the family Epistomiidae (order Cheilostomata).
In the Mesozoic and the Tertiary cheilostome evolution was
accompanied by the appearance of novelties facilitating or
enhancing responses to environmental change. The highest
plasticity, expressed in the acquisition of effective means of
protection (spines, brood chambers, zooidal polymorphs, frontal shields), various growth forms and constructions of colonies, new reproductive patterns and larval types, as well as high
colonial integration and modular complexity, allowed cheilostomes to compete successfully with other epibionts, making
this order one of the most successful groups of colonial invertebrates. Generally, many of these novelties independently
evolved in other bryozoan clades as well, helping bryozoans to
survive mass extinctions and to remain a dominant group in
most benthic assemblages for over 450 million years.
References
Adiyodi KG, Adiyodi RG (eds) (1989) Reproductive biology of invertebrates, vol 4, Part A: fertilization, development, and parental
care. IBH Publishing Co Pvt Ltd, New Delhi/Bombay/Calcutta/
Oxford
Adiyodi KG, Adiyodi RG (eds) (1990) Reproductive biology of invertebrates, vol 4, Part B: fertilization, development, and parental care.
IBH Publishing Co Pvt Ltd, New Delhi/Bombay/Calcutta/Oxford
Adiyodi RG, Subramoniam T (1983) Arthropoda – Crustacea. In:
Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, vol 1, Oogenesis, oviposition, and oosorption. John Wiley
and Sons, Chichester, pp 443–495
Alatalo P, Berg J, Carl J, D’Asaro CN (1984) Reproduction and development in the lucinid clam Codakia orbicularis (Linne, 1758). Bull
Mar Sci 34(3):424–434
Allen JD, Pernet B (2007) Intermediate modes of larval development:
bridging the gap between planktotrophy and lecithotrophy. Evol
Dev 9(6):643–653
Allman G (1856) A monograph of the fresh-water Polyzoa, including
all the known species, both British and foreign. Ray Society, London
Anderson DT (1973) Embryology and phylogeny in annelids and
arthropods. Pergamon Press, New York
Arias A, Reznick D (2000) Life history of Phalloceros caudimaculatus :
a novel variation on the theme of lifebearing in the family
Poeciliidae. Copeia 2000(3):792–798
Atkins D (1955) The cyphonautes larvae of the Plymouth area and the
metamorphosis of Membranipora membranacea (L.). J Mar Biol
Assoc UK 34:441–449
Balon EK (1991) Probable evolution of the coelacanth’s reproductive
style: lecithotrophy and orally feeding embryos in cichlid fi shes and
in Latimeria chalumnae . Environ Biol Fish 32:249–265
Bancroft AJ (1986) Ovicells in Palaeozoic bryozoan order Fenestrata.
Palaeontology 29(1):155–164
Banta WC (1967) A new species of Victorella from Southern California
(Bryozoa, Ctenostomata). Proc US Natl Mus 122(3593):1–18
Banta WC (1968) Mimosella cookae , new species (Bryozoa,
Ctenostomata) with a review of the family Mimosellidae. Bull
South Calif Acad Sci 67:245–254
Barrera E, Savin SM (1999) Evolution of the Late CampanianMaastrichtian marine climates and oceans. In: Barrera E, Johnston
CC (eds) Evolution of the Cretaceous ocean-climate system.
Geological Society of America, Boulder, pp 245–282
Barrois J (1877) Recherches sur l’embryologie des bryozoaires. Trav St
Zool Wimereux 1:1–305
Batygina TB, Bragina EA, Ereskovsky AV, Ostrovsky AN (2006)
Viviparity in plants and animals: invertebrates and lower chordates.
Unipress, St Petersburg State University, St Petersburg [in Russian
with English summary]
Bermingham J, Wilkinson TL (2009) Embryo nutrition in parthenogenetic viviparous aphids. Physiol Entomol 34:103–109
Bishop JDD, Pemberton AJ (2006) The third way: spermcast mating in
sessile marine invertebrates. Integr Comp Biol 46:398–406
Bishop JDD, Manríquez PH, Hughes RN (2000) Water-borne sperm
trigger vitellogenic egg growth in two sessile marine invertebrates.
Proc R Soc B 267:1165–1169
Blackburn DG (1992) Convergent evolution of viviparity, matrotrophy,
and specializations for fetal nutrition in reptiles and other vertebrates. Am Zool 32(2):313–321
Blackburn DG (1993) Chorioallantoic placentation in squamate reptiles
– structure, function, development and evolution. J Exp Zool
266:414–430
Blackburn DG (1994) Standardized criteria for the recognition of
embryonic nutritional patterns in squamate reptiles. Copeia
4:925–935
Blackburn DG (1999a) Viviparity and oviparity: evolution and reproductive strategies. In: Knobil E, Neill JD (eds) Encyclopedia of
reproduction. Academic Press, New York, pp 994–1003
Blackburn DG (1999b) Placenta and placental analogs in reptiles and
amphibians. In: Knobil E, Neill JD (eds) Encyclopedia of reproduction. Academic Press, New York, pp 840–847
Blackburn DG (1999c) Are viviparity and egg-guarding evolutionarily
labile in squamates? Herpetologica 55:556–572
3 Evolution of Reproductive Patterns in Cheilostomata