231
The transition from a planktotrophic to a lecithotrophic
larva and direct development in sea urchins, brittle stars and
sea stars, along with associated changes in embryogenesis,
larval morphology and ecology, were analyzed in detail in the
works of Byrne ( 1991a , b ), Wray ( 1996 ), Hart ( 1996 ) and
McEdward and Janies ( 1993 , 1997 ) (see also McEdward
2000 ; McEdward and Miner 2001 ; Byrne 2006 ). An intermediate stage between feeding and non-feeding modes might be
a form of facultative planktotrophy, known in a number of
invertebrates (discussed in Havenhand 1995 ; Hart 1996 ).
Vance’s ( 1973 ) mathematical model predicts that such a stage
would be of short duration at the geological scale because it is
evolutionarily less successful, as indicated by the fact that
such examples are rare (see also Emlet et al. 1987 ; Wray and
Raff 1991 ; Wray 1995a , 1996 ). It is also possible that their
apparent rarity (as the consequence of a relatively short
evolutionary existence) is because such species either give
rise to species with non-feeding larvae or become extinct
(Wray and Raff 1991 ). Conversely, Emlet ( 1986 ) thought that
facultative planktotrophy may be stable from an evolutionary
viewpoint, as such larvae may profi t from the positive attributes of both developmental variants (Emlet et al. 1987 ;
Havenhand 1995 ; McEdward 1997 ; Allen and Pernet 2007 ;
for a detailed discussion see Hart 1996 ). Wray ( 1996 )
remarked that such larvae are effi cacious only under quite
specifi c conditions. Whatever the case, it is facultative planktotrophy (which according to some researchers is more common than generally thought) that illustrates the transition
from one state to the other (Kempf and Hadfi eld 1985 ; Emlet
1986 ; McEdward 1996 , 1997 ; Allen and Pernet 2007 ).
Among invertebrates, facultative planktotrophy is known
in two sea urchins, four gastropods, a bivalve and a polychaete (Perron 1981 ; Alatalo et al. 1984 ; Kempf and Hadfi eld
1985 ; Emlet 1986 ; Kempf and Todd 1989 ; Miller 1993 ; Hart
1996 ; Pernet and McArthur 2006 ; reviewed in Wray and
Raff 1991 ; Havenhand 1995 ; Wray 1995a ; Raff 1996 ;
Hadfi eld and Strathmann 1996 ). For instance, females of the
polychaete Streblospio benedicti (Atlantic population) form
two types of eggs (small and large), from which, correspondingly, planktotrophic and facultatively planktotrophic larvae
develop. An individual female produces only one type of
oocytes, yet females of different “types” coexist side by side
in the same sites throughout the year. Females from the
Pacifi c population of the same species form only facultative
planktotrophic larvae (Pernet and McArthur 2006 ).
In general, accumulation of additional resources infl uences oocyte size. Havenhand ( 1995 ) and Wray ( 1996 )
considered increase in egg size to be a factor determining the
transition to facultative larval feeding. As egg reserves reach
the threshold required for completion of metamorphosis, this
increase should result in obligate lecithotrophy; many
authors have pointed to the correlation between larval
type and the size of the oocytes from which they develop.
Although this correlation is not strict, an increase in egg size
generally “seems to be both necessary and suffi cient for
completion of metamorphosis without feeding” (reviewed in
Strathmann 1978a , 1993 ; Todd and Doyle 1981 ; Emlet et al.
1987 ; Wray and Raff 1991 ; Wray 1995a , p. 428; Raff 1996 ;
Moran and McAlister 2009 ; see also below).
Thorson ( 1950 ) was one of the fi rst to note the connection
between oocyte size and larval-development type: within a
phylum, small eggs usually develop into planktotrophic
larvae, while large eggs develop into endotrophic larvae or
undergo direct development. Indeed, oocyte size often reliably predicts larval type (Strathmann 1985 ; Jaeckle 1995 ;
Wray 1995a ). In polychaetes of the genus Streblospio , for
instance, oocytes less than 70 μm diameter develop into
planktotrophic larvae and oocytes more than 120 μm into
lecithotrophic larvae. Eggs 200 μm diameter transform
directly into juveniles (reviewed in Levin and Bridges 1995 ).
A similar tendency has been noted within Echinodermata in
general and Echinoidea in particular. In sea urchins, planktotrophic plutei larvae develop from oocytes 65–320 μm diameter, lecithotrophic larvae similar to plutei from oocytes
300–500 μm diameter, strongly modifi ed lecithotrophic larvae from oocytes 400–1,200 μm diameter, and if oocytes
reach 1–2 cm in diameter development is direct (Wray and
Raff 1991 ; Wray 1995a ; Raff 1996 ; Kasyanov 1989 ; Emlet
1990 ; reviewed in Emlet et al. 1987 ). Similar correlations
were recorded in asterinid sea stars in which planktotrophic
larvae develop from 150 to 170 μm eggs and lecithotrophic
ones from 320 to 1,000 μm eggs (reviewed in Emlet et al.
1987 ; Byrne 2006 ; see also Levin and Bridges 1995 ; Jaeckle
1995 ). The larger the oocyte, the fewer traces of planktotrophy are exhibited in echinoderm lecithotrophic larvae (Pearse
and Cameron 1991 ). The same correlation has been ascertained in nudibranch and bivalve molluscs (discussed in
Todd and Doyle 1981 ; Kasyanov 1989 ; Kasyanov et al.
1998 ), and phoronids (Emig 1983 ; Zimmer 1991 ). A similar
correlation was recently shown for Annelida, Echinodermata
and Mollusca by Marshall et al. ( 2012 ).
In this connection, the experiments of Sinervo and
McEdward ( 1988 ) on blastomeres of sea urchins with
planktotrophic development should also be mentioned.
Development of embryos from isolated blastomeres taken
after the fi rst and second divisions (correspondingly ½ and ¼
of zygote volume) of the larger of two congeneric species,
Strongylocentrotus droebachiensis , was slower than the
development of the embryo from the zygote and resulted in a
smaller, simpler larva, comparable with that of the smaller
species S . purpuratus . This means that the size of the initial
cell directly infl uenced the rate and outcome of development.
These authors concluded that the very fact of evolutionary
changes in egg size could be a factor determining the shape
and functions of the larva. According with this conclusion are
the data of Hart ( 1996 ), supporting the hypothesis that, in the
3.1 Modifi cation of Oogenesis and Its Evolutionary Consequences
The transition from a planktotrophic to a lecithotrophic
larva and direct development in sea urchins, brittle stars and
sea stars, along with associated changes in embryogenesis,
larval morphology and ecology, were analyzed in detail in the
works of Byrne ( 1991a , b ), Wray ( 1996 ), Hart ( 1996 ) and
McEdward and Janies ( 1993 , 1997 ) (see also McEdward
2000 ; McEdward and Miner 2001 ; Byrne 2006 ). An intermediate stage between feeding and non-feeding modes might be
a form of facultative planktotrophy, known in a number of
invertebrates (discussed in Havenhand 1995 ; Hart 1996 ).
Vance’s ( 1973 ) mathematical model predicts that such a stage
would be of short duration at the geological scale because it is
evolutionarily less successful, as indicated by the fact that
such examples are rare (see also Emlet et al. 1987 ; Wray and
Raff 1991 ; Wray 1995a , 1996 ). It is also possible that their
apparent rarity (as the consequence of a relatively short
evolutionary existence) is because such species either give
rise to species with non-feeding larvae or become extinct
(Wray and Raff 1991 ). Conversely, Emlet ( 1986 ) thought that
facultative planktotrophy may be stable from an evolutionary
viewpoint, as such larvae may profi t from the positive attributes of both developmental variants (Emlet et al. 1987 ;
Havenhand 1995 ; McEdward 1997 ; Allen and Pernet 2007 ;
for a detailed discussion see Hart 1996 ). Wray ( 1996 )
remarked that such larvae are effi cacious only under quite
specifi c conditions. Whatever the case, it is facultative planktotrophy (which according to some researchers is more common than generally thought) that illustrates the transition
from one state to the other (Kempf and Hadfi eld 1985 ; Emlet
1986 ; McEdward 1996 , 1997 ; Allen and Pernet 2007 ).
Among invertebrates, facultative planktotrophy is known
in two sea urchins, four gastropods, a bivalve and a polychaete (Perron 1981 ; Alatalo et al. 1984 ; Kempf and Hadfi eld
1985 ; Emlet 1986 ; Kempf and Todd 1989 ; Miller 1993 ; Hart
1996 ; Pernet and McArthur 2006 ; reviewed in Wray and
Raff 1991 ; Havenhand 1995 ; Wray 1995a ; Raff 1996 ;
Hadfi eld and Strathmann 1996 ). For instance, females of the
polychaete Streblospio benedicti (Atlantic population) form
two types of eggs (small and large), from which, correspondingly, planktotrophic and facultatively planktotrophic larvae
develop. An individual female produces only one type of
oocytes, yet females of different “types” coexist side by side
in the same sites throughout the year. Females from the
Pacifi c population of the same species form only facultative
planktotrophic larvae (Pernet and McArthur 2006 ).
In general, accumulation of additional resources infl uences oocyte size. Havenhand ( 1995 ) and Wray ( 1996 )
considered increase in egg size to be a factor determining the
transition to facultative larval feeding. As egg reserves reach
the threshold required for completion of metamorphosis, this
increase should result in obligate lecithotrophy; many
authors have pointed to the correlation between larval
type and the size of the oocytes from which they develop.
Although this correlation is not strict, an increase in egg size
generally “seems to be both necessary and suffi cient for
completion of metamorphosis without feeding” (reviewed in
Strathmann 1978a , 1993 ; Todd and Doyle 1981 ; Emlet et al.
1987 ; Wray and Raff 1991 ; Wray 1995a , p. 428; Raff 1996 ;
Moran and McAlister 2009 ; see also below).
Thorson ( 1950 ) was one of the fi rst to note the connection
between oocyte size and larval-development type: within a
phylum, small eggs usually develop into planktotrophic
larvae, while large eggs develop into endotrophic larvae or
undergo direct development. Indeed, oocyte size often reliably predicts larval type (Strathmann 1985 ; Jaeckle 1995 ;
Wray 1995a ). In polychaetes of the genus Streblospio , for
instance, oocytes less than 70 μm diameter develop into
planktotrophic larvae and oocytes more than 120 μm into
lecithotrophic larvae. Eggs 200 μm diameter transform
directly into juveniles (reviewed in Levin and Bridges 1995 ).
A similar tendency has been noted within Echinodermata in
general and Echinoidea in particular. In sea urchins, planktotrophic plutei larvae develop from oocytes 65–320 μm diameter, lecithotrophic larvae similar to plutei from oocytes
300–500 μm diameter, strongly modifi ed lecithotrophic larvae from oocytes 400–1,200 μm diameter, and if oocytes
reach 1–2 cm in diameter development is direct (Wray and
Raff 1991 ; Wray 1995a ; Raff 1996 ; Kasyanov 1989 ; Emlet
1990 ; reviewed in Emlet et al. 1987 ). Similar correlations
were recorded in asterinid sea stars in which planktotrophic
larvae develop from 150 to 170 μm eggs and lecithotrophic
ones from 320 to 1,000 μm eggs (reviewed in Emlet et al.
1987 ; Byrne 2006 ; see also Levin and Bridges 1995 ; Jaeckle
1995 ). The larger the oocyte, the fewer traces of planktotrophy are exhibited in echinoderm lecithotrophic larvae (Pearse
and Cameron 1991 ). The same correlation has been ascertained in nudibranch and bivalve molluscs (discussed in
Todd and Doyle 1981 ; Kasyanov 1989 ; Kasyanov et al.
1998 ), and phoronids (Emig 1983 ; Zimmer 1991 ). A similar
correlation was recently shown for Annelida, Echinodermata
and Mollusca by Marshall et al. ( 2012 ).
In this connection, the experiments of Sinervo and
McEdward ( 1988 ) on blastomeres of sea urchins with
planktotrophic development should also be mentioned.
Development of embryos from isolated blastomeres taken
after the fi rst and second divisions (correspondingly ½ and ¼
of zygote volume) of the larger of two congeneric species,
Strongylocentrotus droebachiensis , was slower than the
development of the embryo from the zygote and resulted in a
smaller, simpler larva, comparable with that of the smaller
species S . purpuratus . This means that the size of the initial
cell directly infl uenced the rate and outcome of development.
These authors concluded that the very fact of evolutionary
changes in egg size could be a factor determining the shape
and functions of the larva. According with this conclusion are
the data of Hart ( 1996 ), supporting the hypothesis that, in the
3.1 Modifi cation of Oogenesis and Its Evolutionary Consequences