232
transition from feeding to non-feeding mode, evolution of
large eggs precedes any modifi cations in larval development.
However, this rule does not appear to be very strict. There
are cases among sea urchins in which non-feeding larvae
develop from smaller oocytes, whereas echinoplutei develop
from larger ones (Emlet et al. 1987 ; Bosch 1989 ; Wray and
Raff 1991 ; Hoegh-Guldberg and Pearse 1995 ). To sum up,
there is a general correlation between larger eggs and lecithotrophy but there are exceptions. This conclusion is supported by experimental embryological data: in the sea urchin
Peronella japonica a lecithotrophic larva develops from each
of the two blastomeres separated after the fi rst division (as it
does from the normal embryo), though these blastomeres are
much smaller than the oocytes of planktotrophic species
(Okazaki and Dan 1954 ; Wray and Raff 1991 ; summarized
in Jaeckle 1995 ). A similar situation obtains for half-embryos
resulting from bisection along the second cleavage plane of
Heliocidaris erythrogramma (Henry and Raff 1990 ; Wray
and Raff 1991 ). The developmental programme appears to
be genetically determined in these species.
Oocytes of invertebrates differ not only in size but also in
the content of a particular nutrient per unit volume, with
small oocytes being characterized by higher concentrations
than large ones in echinoderms with feeding larvae
(Strathmann and Vedder 1977 ). Thus, differences between
two contrasting developmental modes cannot be simply
explained by the absolute size of the egg. What is very
important is the amount of organic content (McEdward and
Carson 1987 ) and biochemical composition (Jaeckle 1995 ),
hence egg volume is not simply proportional to its energy
content (Emlet et al. 1987 ; Eckelbarger 1994 ). It has been
shown in echinoderms that planktotrophic larvae develop
from the oocytes that mostly accumulate proteins, while lecithotrophic ones develop from those that accumulate lipids.
The evolution of large eggs, in concert with transition to the
preferred and progressive accumulation of lipids in oocytes,
is considered to be an important aspect of the transformation
of oogenesis during evolution of lecithotrophic larvae (Wray
and Raff 1991 ; Byrne et al. 1999 , 2003 ; Byrne and Cerra
2000 ; Villinski et al. 2002 ; Wray 2002 ; Falkner et al. 2006 ;
Prowse et al. 2008 , 2009 ).
According to Christiansen and Fenchel ( 1979 ), the transition from one developmental type to the other may be rather
fast by geological standards, as little as several million years
(see also Wray and Raff 1991 ; Wray 1995a , b ). This transition was accomplished in four to seven million years in two
clades of sea urchins living on different sides of the Isthmus
of Panama (Zigler et al. 2003 ; Jeffery et al. 2003 , discussed in
Raff and Byrne 2006 ). Moreover, Hart et al. ( 1997 ) presented
molecular data showing that it might take less than two
million years in sea stars. Strathmann and Eernisse ( 1994 )
agreed that an increase in nutritional reserves in the ovum
would permit rapid evolutionary changes in larval form.
Instances of congeneric species having exo- and endotrophic
larvae are well-known in sea urchins, sea stars, polychaetes,
ctenostome bryozoans and some other invertebrates;
moreover, in some opisthobranch gastropods and polychaetes these two types of larvae may be found within the
same species (poecilogony) (Zimmer and Woollacott
1977a ; Clark et al. 1979 ; Hoagland and Robertson 1988 ;
Pearse and Cameron 1991 ; Wray and Raff 1991 ; Byrne
1991b , 2006 ; Byrne and Barker 1991 ; Levin and Bridges
1995 ; Havenhand 1995 ; Raff 1996 ; Hart 1996 ; Byrne et al.
1999 ; Gibson and Gibson 2004 ; Krug 2007 ). These
instances indicate that the switch from one oogenesis
type to the other, which occurred repeatedly in the history
of different groups and hence from one larval type to the
other, is not a very diffi cult evolutionary step. A striking
example is provided by the snail Alderia willowi , which
shifts oogenesis (and hence larval type) depending on the
season: numerous small eggs from which long-living
planktotrophic larvae develop are produced in winter and
spring, whereas a few large eggs from which lecithotrophic
larvae develop are laid in summer. Moreover, some nonfeeding larvae undergo metamorphosis immediately after
hatching and some settle only 2–4 days later. In addition,
the same snails may switch from one type of oogenesis
(and larva) to the other (Ellingson and Krug 2006 ; Krug 2007 ;
Krug et al. 2007 ).
In discussing genetic changes behind the loss of larval
characters, Nielsen ( 1998 , p. 144) wrote that there might be
only a single mutation in larval development “which turns
off the regulatory gene”. In contrast, Strathmann with coauthors ( 1992 ) inferred that the main reason is a genetic
change in the programming of oogenesis. It was shown in
experiments using sea urchin planktotrophic larvae that
abundance of food results in both shortening of development
time and changes in the structure and development of the
plutei. Moreover, such plutei structurally and developmentally resembled sea urchin endotrophic larvae. This phenotypic plasticity was considered as a preadaptation in the
transition to a non-feeding larva. Based on this, Strathmann
and coauthors ( 1992 ) suggested that regardless of whether
nutrient resources are exo- or endogenous an increase in
their amount would result in structural changes in the larvae
enabling the fastest possible competence. In their opinion,
since the plentiful food available for planktotrophic larvae
results in changes characteristic of lecithotrophic ones, the
transition to non-feeding larvae does not require genetic
changes relating to embryogenesis and larval development.
Changes in the genetic programme of oogenesis that result
in an increase in the amount of nutrients in the oocytes is
suffi cient. According to Wray and Raff ( 1991 ), the necessary
prerequisite for a transition to a new larval type is the “weakening” of the pressure of stabilizing selection and the accumulation of mutations.
3 Evolution of Reproductive Patterns in Cheilostomata
transition from feeding to non-feeding mode, evolution of
large eggs precedes any modifi cations in larval development.
However, this rule does not appear to be very strict. There
are cases among sea urchins in which non-feeding larvae
develop from smaller oocytes, whereas echinoplutei develop
from larger ones (Emlet et al. 1987 ; Bosch 1989 ; Wray and
Raff 1991 ; Hoegh-Guldberg and Pearse 1995 ). To sum up,
there is a general correlation between larger eggs and lecithotrophy but there are exceptions. This conclusion is supported by experimental embryological data: in the sea urchin
Peronella japonica a lecithotrophic larva develops from each
of the two blastomeres separated after the fi rst division (as it
does from the normal embryo), though these blastomeres are
much smaller than the oocytes of planktotrophic species
(Okazaki and Dan 1954 ; Wray and Raff 1991 ; summarized
in Jaeckle 1995 ). A similar situation obtains for half-embryos
resulting from bisection along the second cleavage plane of
Heliocidaris erythrogramma (Henry and Raff 1990 ; Wray
and Raff 1991 ). The developmental programme appears to
be genetically determined in these species.
Oocytes of invertebrates differ not only in size but also in
the content of a particular nutrient per unit volume, with
small oocytes being characterized by higher concentrations
than large ones in echinoderms with feeding larvae
(Strathmann and Vedder 1977 ). Thus, differences between
two contrasting developmental modes cannot be simply
explained by the absolute size of the egg. What is very
important is the amount of organic content (McEdward and
Carson 1987 ) and biochemical composition (Jaeckle 1995 ),
hence egg volume is not simply proportional to its energy
content (Emlet et al. 1987 ; Eckelbarger 1994 ). It has been
shown in echinoderms that planktotrophic larvae develop
from the oocytes that mostly accumulate proteins, while lecithotrophic ones develop from those that accumulate lipids.
The evolution of large eggs, in concert with transition to the
preferred and progressive accumulation of lipids in oocytes,
is considered to be an important aspect of the transformation
of oogenesis during evolution of lecithotrophic larvae (Wray
and Raff 1991 ; Byrne et al. 1999 , 2003 ; Byrne and Cerra
2000 ; Villinski et al. 2002 ; Wray 2002 ; Falkner et al. 2006 ;
Prowse et al. 2008 , 2009 ).
According to Christiansen and Fenchel ( 1979 ), the transition from one developmental type to the other may be rather
fast by geological standards, as little as several million years
(see also Wray and Raff 1991 ; Wray 1995a , b ). This transition was accomplished in four to seven million years in two
clades of sea urchins living on different sides of the Isthmus
of Panama (Zigler et al. 2003 ; Jeffery et al. 2003 , discussed in
Raff and Byrne 2006 ). Moreover, Hart et al. ( 1997 ) presented
molecular data showing that it might take less than two
million years in sea stars. Strathmann and Eernisse ( 1994 )
agreed that an increase in nutritional reserves in the ovum
would permit rapid evolutionary changes in larval form.
Instances of congeneric species having exo- and endotrophic
larvae are well-known in sea urchins, sea stars, polychaetes,
ctenostome bryozoans and some other invertebrates;
moreover, in some opisthobranch gastropods and polychaetes these two types of larvae may be found within the
same species (poecilogony) (Zimmer and Woollacott
1977a ; Clark et al. 1979 ; Hoagland and Robertson 1988 ;
Pearse and Cameron 1991 ; Wray and Raff 1991 ; Byrne
1991b , 2006 ; Byrne and Barker 1991 ; Levin and Bridges
1995 ; Havenhand 1995 ; Raff 1996 ; Hart 1996 ; Byrne et al.
1999 ; Gibson and Gibson 2004 ; Krug 2007 ). These
instances indicate that the switch from one oogenesis
type to the other, which occurred repeatedly in the history
of different groups and hence from one larval type to the
other, is not a very diffi cult evolutionary step. A striking
example is provided by the snail Alderia willowi , which
shifts oogenesis (and hence larval type) depending on the
season: numerous small eggs from which long-living
planktotrophic larvae develop are produced in winter and
spring, whereas a few large eggs from which lecithotrophic
larvae develop are laid in summer. Moreover, some nonfeeding larvae undergo metamorphosis immediately after
hatching and some settle only 2–4 days later. In addition,
the same snails may switch from one type of oogenesis
(and larva) to the other (Ellingson and Krug 2006 ; Krug 2007 ;
Krug et al. 2007 ).
In discussing genetic changes behind the loss of larval
characters, Nielsen ( 1998 , p. 144) wrote that there might be
only a single mutation in larval development “which turns
off the regulatory gene”. In contrast, Strathmann with coauthors ( 1992 ) inferred that the main reason is a genetic
change in the programming of oogenesis. It was shown in
experiments using sea urchin planktotrophic larvae that
abundance of food results in both shortening of development
time and changes in the structure and development of the
plutei. Moreover, such plutei structurally and developmentally resembled sea urchin endotrophic larvae. This phenotypic plasticity was considered as a preadaptation in the
transition to a non-feeding larva. Based on this, Strathmann
and coauthors ( 1992 ) suggested that regardless of whether
nutrient resources are exo- or endogenous an increase in
their amount would result in structural changes in the larvae
enabling the fastest possible competence. In their opinion,
since the plentiful food available for planktotrophic larvae
results in changes characteristic of lecithotrophic ones, the
transition to non-feeding larvae does not require genetic
changes relating to embryogenesis and larval development.
Changes in the genetic programme of oogenesis that result
in an increase in the amount of nutrients in the oocytes is
suffi cient. According to Wray and Raff ( 1991 ), the necessary
prerequisite for a transition to a new larval type is the “weakening” of the pressure of stabilizing selection and the accumulation of mutations.
3 Evolution of Reproductive Patterns in Cheilostomata