230
3.1
Modifi cation of Oogenesis and
Its Evolutionary Consequences
3.1.1 Changes in Oogenesis and Evolution
of the Lecithotrophic Larva
3.1.1.1 General Remarks
Planktotrophy is considered as the primitive state of the
larval phase in the life cycle of marine invertebrates
(Jägersten 1972 ; Strathmann 1978a , b ; Nielsen 1998 , 2013 ;
Levin and Bridges 1995 ; Wray 1995a ), though there are
strong arguments supporting the opinion that the fi rst larval
forms of early metazoans were non-feeding (von SalviniPlawen 1982 ; Haszprunar et al. 1995 ; Peterson 2005 ; Nützel
et al. 2006 ; see also Strathmann 1993 ). Still, planktotrophic
larvae are very ancient, and it is generally accepted that the
transition to endotrophy occurred repeatedly in many marine
phyla (Jägersten 1972 ; Strathmann 1975 , 1978a , 1985 , 1986 ,
1993 ; Wray 1995a ; McEdward and Janies 1997 ; Nielsen
1998 , 2013 ; Peterson 2005 and references therein). For
instance, in the phylum Echinodermata this transition
occurred at least 35 times (Emlet et al. 1987 ; Wray 1995a )
and within the sea star family Asterinidae lecithotrophy
originated independently six times (Byrne 2006 ).
Hypothetical consequences of the evolution of nonfeeding larva are discussed in numerous publications (see
Chia 1974 ; Strathmann 1978a , 1980 , 1985 ; Jablonski and
Lutz 1983 ; Jablonski 1986 ; Emlet et al. 1987 ; Poulin and
Féral 1996 and references therein). On the whole, such larvae,
with their lesser dependence on external conditions and
lesser risk of mortality because of a generally shorter swimming period, are considered as an alternative to widerdispersing larvae with a prolonged feeding in the plankton.
The necessity of dispersal vs the “expediency” of progeny
settling in the biotopes where the parents live has also been
broadly discussed (for reviews see Strathmann 1985 ;
Kasyanov 1989 ; Reed 1991 ; Knowlton and Jackson 1993 ;
Havenhand 1995 ).
There are a number of hypotheses discussing ecological
factors that might trigger the transition from exotrophy to
endotrophy (reviewed in Strathmann 1985 , 1986 ; Havenhand
1995 ; Levin and Bridges 1995 ). For instance, fl uctuations in
phytoplankton abundance owing to climatic seasonality are
often considered. When the amount of food accessible to
planktotrophic larvae fl uctuates abruptly, a transition to
lecithotrophy does seem benefi cial (McNamara 1994 ; Poulin
and Féral 1996 ; Jeffery 1997 ; McEdward and Miner 2003 ;
see also Valentine 1986 ). This hypothesis is rooted in
Thorson’s rule (so-called), suggesting that planktotrophic
development is rare in cold (i.e. polar and deep) waters.
(Thorson 1950 ; Mileikovsky 1971 ; Clarke 1992 ; Jablonski
and Lutz 1983 ; Kasyanov 1989 ). Although Thorson’s rule
itself was strongly criticized (Chia 1974 ; Clark and Goetzfried
1978 ; Pearse 1994 ; Pearse and Bosch 1994 ; see also Levin and
Bridges 1995 and Marshall et al. 2012 ), a correlation between
trophic limitations and the shift to a non-feeding larva still
seems theoretically reasonable (Clarke 1992 ; Jeffery 1997 ).
Other hypotheses explain a loss of planktotrophy by
seasonal freshening of surface waters after ice melting, low
temperatures (in high latitudes) and dispersal features, etc.
(discussed in Poulin and Féral 1996 ). According to Chia
( 1974 ), transition to lecithotrophy can be a forced response
to having to survive conditions of acute resource shortage for
adults. In this case a decrease in the number of offspring is
effi cacious, being offset by larger offspring size and thus
lesser vulnerability to predation. Nielsen ( 1995 , 1998 )
argued that non-feeding larvae could have evolved as a result
of competition and/or predation in the plankton. Todd and
Doyle ( 1981 ) suggested that the evolution of new larval
types could be associated with the timing of reproduction
and settlement periods in relation to seasons having an
increased amount of food available to parents and juveniles,
the type of larva and the duration of its development
depending on the availability of food for the juvenile (see
also Havenhand 1993 ).
The above hypotheses suggest that ecology drives the shift
in larval type. But what are the intrinsic mechanisms behind
this shift? It has been accepted relatively recently that “it is
during oogenesis that the developmental program is altered
and saved both in terms of nuclear genetic information and in
the cytoplasmic organization of the egg” (Raff and Kaufman
1983 ; Wourms 1987 , p. 52; Wray and Raff 1991 ; Raff 1996 ;
see also Prowse and Byrne 2012 ) and that the transition from
one larval type to another involves correlated changes in
oogenesis, embryogenesis and larval development (Wray and
Raff 1990 , 1991 ; Wray 1992 ; Eckelbarger 1994 ).
Whatever the ecological factors and selective regimes in
the evolution of a non-feeding mode of development, the
necessary step in this direction was modifi cation of oogenesis via an increase in the maternal provisioning that resulted
in a larger, nutrient-rich oocyte (Wray and Raff 1991 ; Jaeckle
1995 ; Byrne et al. 2003 ). Chia ( 1974 ) and Strathmann and
co-authors ( 1992 ) noted that the evolution of lecithotrophy
might be explained by an increase in the energy input of
the parent organism into oocyte development. In this way,
the offspring would have been provisioned with suffi cient
reserves to complete development without feeding
(Mortensen 1921 ; Havenhand 1995 ; Wray 1995a ). As a
result, the larvae formed from large oocytes no longer
needed structures for capture and digestion of food particles
(Strathmann 1978a , 1993 ). As Strathmann ( 1975 , p. 727)
wrote: “if an egg is supplied with suffi cient reserves so that
feeding is no longer required for completion of larval
development, then selection will no longer eliminate many
mutations affecting the development of the larval body.”
3 Evolution of Reproductive Patterns in Cheilostomata
3.1
Modifi cation of Oogenesis and
Its Evolutionary Consequences
3.1.1 Changes in Oogenesis and Evolution
of the Lecithotrophic Larva
3.1.1.1 General Remarks
Planktotrophy is considered as the primitive state of the
larval phase in the life cycle of marine invertebrates
(Jägersten 1972 ; Strathmann 1978a , b ; Nielsen 1998 , 2013 ;
Levin and Bridges 1995 ; Wray 1995a ), though there are
strong arguments supporting the opinion that the fi rst larval
forms of early metazoans were non-feeding (von SalviniPlawen 1982 ; Haszprunar et al. 1995 ; Peterson 2005 ; Nützel
et al. 2006 ; see also Strathmann 1993 ). Still, planktotrophic
larvae are very ancient, and it is generally accepted that the
transition to endotrophy occurred repeatedly in many marine
phyla (Jägersten 1972 ; Strathmann 1975 , 1978a , 1985 , 1986 ,
1993 ; Wray 1995a ; McEdward and Janies 1997 ; Nielsen
1998 , 2013 ; Peterson 2005 and references therein). For
instance, in the phylum Echinodermata this transition
occurred at least 35 times (Emlet et al. 1987 ; Wray 1995a )
and within the sea star family Asterinidae lecithotrophy
originated independently six times (Byrne 2006 ).
Hypothetical consequences of the evolution of nonfeeding larva are discussed in numerous publications (see
Chia 1974 ; Strathmann 1978a , 1980 , 1985 ; Jablonski and
Lutz 1983 ; Jablonski 1986 ; Emlet et al. 1987 ; Poulin and
Féral 1996 and references therein). On the whole, such larvae,
with their lesser dependence on external conditions and
lesser risk of mortality because of a generally shorter swimming period, are considered as an alternative to widerdispersing larvae with a prolonged feeding in the plankton.
The necessity of dispersal vs the “expediency” of progeny
settling in the biotopes where the parents live has also been
broadly discussed (for reviews see Strathmann 1985 ;
Kasyanov 1989 ; Reed 1991 ; Knowlton and Jackson 1993 ;
Havenhand 1995 ).
There are a number of hypotheses discussing ecological
factors that might trigger the transition from exotrophy to
endotrophy (reviewed in Strathmann 1985 , 1986 ; Havenhand
1995 ; Levin and Bridges 1995 ). For instance, fl uctuations in
phytoplankton abundance owing to climatic seasonality are
often considered. When the amount of food accessible to
planktotrophic larvae fl uctuates abruptly, a transition to
lecithotrophy does seem benefi cial (McNamara 1994 ; Poulin
and Féral 1996 ; Jeffery 1997 ; McEdward and Miner 2003 ;
see also Valentine 1986 ). This hypothesis is rooted in
Thorson’s rule (so-called), suggesting that planktotrophic
development is rare in cold (i.e. polar and deep) waters.
(Thorson 1950 ; Mileikovsky 1971 ; Clarke 1992 ; Jablonski
and Lutz 1983 ; Kasyanov 1989 ). Although Thorson’s rule
itself was strongly criticized (Chia 1974 ; Clark and Goetzfried
1978 ; Pearse 1994 ; Pearse and Bosch 1994 ; see also Levin and
Bridges 1995 and Marshall et al. 2012 ), a correlation between
trophic limitations and the shift to a non-feeding larva still
seems theoretically reasonable (Clarke 1992 ; Jeffery 1997 ).
Other hypotheses explain a loss of planktotrophy by
seasonal freshening of surface waters after ice melting, low
temperatures (in high latitudes) and dispersal features, etc.
(discussed in Poulin and Féral 1996 ). According to Chia
( 1974 ), transition to lecithotrophy can be a forced response
to having to survive conditions of acute resource shortage for
adults. In this case a decrease in the number of offspring is
effi cacious, being offset by larger offspring size and thus
lesser vulnerability to predation. Nielsen ( 1995 , 1998 )
argued that non-feeding larvae could have evolved as a result
of competition and/or predation in the plankton. Todd and
Doyle ( 1981 ) suggested that the evolution of new larval
types could be associated with the timing of reproduction
and settlement periods in relation to seasons having an
increased amount of food available to parents and juveniles,
the type of larva and the duration of its development
depending on the availability of food for the juvenile (see
also Havenhand 1993 ).
The above hypotheses suggest that ecology drives the shift
in larval type. But what are the intrinsic mechanisms behind
this shift? It has been accepted relatively recently that “it is
during oogenesis that the developmental program is altered
and saved both in terms of nuclear genetic information and in
the cytoplasmic organization of the egg” (Raff and Kaufman
1983 ; Wourms 1987 , p. 52; Wray and Raff 1991 ; Raff 1996 ;
see also Prowse and Byrne 2012 ) and that the transition from
one larval type to another involves correlated changes in
oogenesis, embryogenesis and larval development (Wray and
Raff 1990 , 1991 ; Wray 1992 ; Eckelbarger 1994 ).
Whatever the ecological factors and selective regimes in
the evolution of a non-feeding mode of development, the
necessary step in this direction was modifi cation of oogenesis via an increase in the maternal provisioning that resulted
in a larger, nutrient-rich oocyte (Wray and Raff 1991 ; Jaeckle
1995 ; Byrne et al. 2003 ). Chia ( 1974 ) and Strathmann and
co-authors ( 1992 ) noted that the evolution of lecithotrophy
might be explained by an increase in the energy input of
the parent organism into oocyte development. In this way,
the offspring would have been provisioned with suffi cient
reserves to complete development without feeding
(Mortensen 1921 ; Havenhand 1995 ; Wray 1995a ). As a
result, the larvae formed from large oocytes no longer
needed structures for capture and digestion of food particles
(Strathmann 1978a , 1993 ). As Strathmann ( 1975 , p. 727)
wrote: “if an egg is supplied with suffi cient reserves so that
feeding is no longer required for completion of larval
development, then selection will no longer eliminate many
mutations affecting the development of the larval body.”
3 Evolution of Reproductive Patterns in Cheilostomata