Chapter 12
REPRODUCTION, DEVELOPMENT AND LIFE-HISTORY TRAITS
Craig M. YOUNG
INTRODUCTION
From the earliest days of deep-sea exploration, it
was assumed that animals living in the presumably
“hostile” environments of the deep sea should show
life-history attributes and reproductive modes differing
from those of their shallow-water counterparts. Shortly
after the Challenger expedition returned from its
circumnavigation of the globe, H.N. Moseley (1880)
one of the naturalists of the expedition, summarized the
current state of knowledge about conditions in the deep
sea. He suggested, as had Wyville Thomson (1878)
before him, that brooding (parental care of offspring)
is a predominant reproductive strategy in deep water.
This idea was supported by the finding of large egg
sizes in echinoderms and cnidarians during the same
expedition (Agassiz, 1881; Moseley, 1881), and set
the stage for a generalization, ultimately formalized as
Thorson’s Rule (Mileikovsky, 1971), which remained
entrenched in the literature until very recent times,
when numerous exceptions have been documented
(reviewed by Young, 1994a; Pearse, 1994). A second
idea first advanced by John Orton (1920) as a testable
but untested hypothesis was that reproduction should
be aperiodic in the constant thermal conditions of the
deep sea. This hypothesis quickly became accepted
as established fact and was questioned only when
deep-sea seasonality and reproductive periodicity were
documented after the 1960s (reviewed by Tyler, 1988).
Both Thorson’s Rule and Orton’s Rule were reasonable hypotheses when the deep sea was thought to be
a completely monotonous habitat with no primary productivity, limited energy and virtually constant physical
and chemical conditions. The predictive power of
both proved inadequate once one began to understand
something of the complexity, dynamics and variability
of the deep-sea environment. Unexpected variability
has been demonstrated dramatically in the past two
decades by the discovery of vents and seeps (see
Chapter 4; Lonsdale, 1977; MacDonald et al., 1989),
benthic storms (Chapter 2; Gardner and Sullivan, 1981;
Hollister and McCave, 1984; Hollister and Nowell,
1991), turbidites (Chapter 2; McCave and Jones, 1988),
and other major sources of disturbance. Nevertheless,
the vertical gradients of environmental stability and
of nutrient availability that provided impetus for the
earliest predictions remain a useful framework for
considering how natural selection has shaped the lifehistory attributes of deep-sea animals.
In this chapter, I provide a phyletic overview of
known reproductive parameters and developmental
modes of deep-sea invertebrates, then apply various
predictions of life-history theory to deep-sea animals,
considering which predictions are supported or refuted
by the available data. Both chemosynthetic and nonchemosynthetic systems are discussed, though the emphasis is on the latter, as a comprehensive summary of
reproduction at hydrothermal vents and cold methane
seeps has recently been published (Tyler and Young,
1999). Space limits the present treatment to benthic
invertebrates; for portals into the literature on lifehistory attributes of deep-sea fishes, the reader is
referred to Stein and Pearcy (1982), Gordon and
Duncan (1985) and Merrett (1987).
PHYLETIC OVERVIEW OF REPRODUCTION AND
DEVELOPMENT
In his seminal review of evolutionary ecology in the
deep sea, Sanders (1977) noted that deep-sea benthic
sediments are dominated by polychaetes, crustaceans,
molluscs (especially protobranch bivalves and gastropods) and echinoderms, the peracarid crustaceans
381
REPRODUCTION, DEVELOPMENT AND LIFE-HISTORY TRAITS
Craig M. YOUNG
INTRODUCTION
From the earliest days of deep-sea exploration, it
was assumed that animals living in the presumably
“hostile” environments of the deep sea should show
life-history attributes and reproductive modes differing
from those of their shallow-water counterparts. Shortly
after the Challenger expedition returned from its
circumnavigation of the globe, H.N. Moseley (1880)
one of the naturalists of the expedition, summarized the
current state of knowledge about conditions in the deep
sea. He suggested, as had Wyville Thomson (1878)
before him, that brooding (parental care of offspring)
is a predominant reproductive strategy in deep water.
This idea was supported by the finding of large egg
sizes in echinoderms and cnidarians during the same
expedition (Agassiz, 1881; Moseley, 1881), and set
the stage for a generalization, ultimately formalized as
Thorson’s Rule (Mileikovsky, 1971), which remained
entrenched in the literature until very recent times,
when numerous exceptions have been documented
(reviewed by Young, 1994a; Pearse, 1994). A second
idea first advanced by John Orton (1920) as a testable
but untested hypothesis was that reproduction should
be aperiodic in the constant thermal conditions of the
deep sea. This hypothesis quickly became accepted
as established fact and was questioned only when
deep-sea seasonality and reproductive periodicity were
documented after the 1960s (reviewed by Tyler, 1988).
Both Thorson’s Rule and Orton’s Rule were reasonable hypotheses when the deep sea was thought to be
a completely monotonous habitat with no primary productivity, limited energy and virtually constant physical
and chemical conditions. The predictive power of
both proved inadequate once one began to understand
something of the complexity, dynamics and variability
of the deep-sea environment. Unexpected variability
has been demonstrated dramatically in the past two
decades by the discovery of vents and seeps (see
Chapter 4; Lonsdale, 1977; MacDonald et al., 1989),
benthic storms (Chapter 2; Gardner and Sullivan, 1981;
Hollister and McCave, 1984; Hollister and Nowell,
1991), turbidites (Chapter 2; McCave and Jones, 1988),
and other major sources of disturbance. Nevertheless,
the vertical gradients of environmental stability and
of nutrient availability that provided impetus for the
earliest predictions remain a useful framework for
considering how natural selection has shaped the lifehistory attributes of deep-sea animals.
In this chapter, I provide a phyletic overview of
known reproductive parameters and developmental
modes of deep-sea invertebrates, then apply various
predictions of life-history theory to deep-sea animals,
considering which predictions are supported or refuted
by the available data. Both chemosynthetic and nonchemosynthetic systems are discussed, though the emphasis is on the latter, as a comprehensive summary of
reproduction at hydrothermal vents and cold methane
seeps has recently been published (Tyler and Young,
1999). Space limits the present treatment to benthic
invertebrates; for portals into the literature on lifehistory attributes of deep-sea fishes, the reader is
referred to Stein and Pearcy (1982), Gordon and
Duncan (1985) and Merrett (1987).
PHYLETIC OVERVIEW OF REPRODUCTION AND
DEVELOPMENT
In his seminal review of evolutionary ecology in the
deep sea, Sanders (1977) noted that deep-sea benthic
sediments are dominated by polychaetes, crustaceans,
molluscs (especially protobranch bivalves and gastropods) and echinoderms, the peracarid crustaceans
381