Discussion
Our systematic map of marine complex life histories identified emphases
and knowledge gaps in the literature. Most studies of life histories
were done in the laboratory on the F0 adult, embryonic
and larval stages in isolation. The most important issue our map
identified was the lack of studies that both explore the entire life
history and follow the same individuals over time. Studies that measured
more than one stage almost exclusively followed cohorts rather than
individuals—following individuals through the life cycle was rare
(1.7%). If we are to better understand the phenotypic links across
life-history stages, free of the potentially confounding influence of
the Simpson’s Paradox, then individual longitudinal studies should be
priority.
Experimental design and stages . The most substantial gap
identified in the systematic map is the underrepresentation of
individual longitudinal studies. Studies that focus on a single stage
make up ~67% of studies in the map, meaning the
literature has focused on characterising life histories, rather than
exploring links between stages. About 31% of studies used a cohort
longitudinal design—following a single cohort is useful for
quantitative genetic studies or when offspring traits of the entire
brood are of interest (e.g. . Our map found that just 1.7% of studies
were individual longitudinal. Individual longitudinal studies have been
suggested as the best approach for addressing many life-history
questions including those on senescence, age-related changes in the life
history, population density regulation and links between stages . An
interesting next step would be to explore whether a lack of individual
longitudinal studies also pervades studies of complex life histories in
terrestrial taxa (e.g. insects). We predict a similar dearth of such
studies in these taxa also.
Answering life-history questions often requires individual longitudinal
studies that measure the entire life history—for example, estimating
lifetime reproductive output between parents and offspring or over
multiple cohorts is ideal for estimating selection on a trait or to
project population dynamics . However, measuring individuals over the
entire life history is rare—long-term studies are costly, logistically
difficult to maintain and, therefore, risky to undertake, particularly
for long-lived species . We found only one case in which all stages of
the life cycle were measured—an individual longitudinal study that
used a species with only four stages (i.e. direct development).
Importantly, we know other studies exist that meet some of our criteria
(and some are even well-known studies), but were not captured by our
systematic map. This highlights an important limitation to systematic
maps that must be acknowledged: no map will be perfectly comprehensive,
so missing some important studies is unavoidable. Expanding search terms
further generated an impractical number of papers to process, as the
17,000+ papers that we did screen required 100s of people-hours.
Nevertheless, our map can be considered a representative and unbiased
sample of the literature such that the relative abundance of different
study types is unlikely to change, were broader terms used. Suffice it
to say, regardless of how they are searched for, individual longitudinal
studies remain rare in the literature.
We find that cohort longitudinal studies measured the F0adult, embryonic and larval stages most often (Figures 4a, 5a). However,
we found the opposite trend in individual longitudinal studies which
measured metamorphs, juveniles and F1 adults most often
(Figure 4c). Why do studies following individuals mostly measure stages
after metamorphosis? Of the studies that used an individual longitudinal
approach, 71% used species with lecithotrophic larvae (i.e. planktonic,
non-feeding), which also have relatively short development times.
Culturing individuals with long development times hinder whole life
cycle studies of those species—for example, it is much more difficult
to study the whole life history of the planktotrophic (i.e. planktonic,
feeding larvae) sea star Pisaster ochraceus , which matures in 5
years , compared to the lecithotrophic marine bryozoan Bugula
neritina , which takes ~7 weeks to mature . Because of
the challenge in executing individual longitudinal studies, our
understanding of links between immature stages and F1adults is largely a black box—only 12 individual longitudinal
experiments in our map measured both juveniles and F1adults, and none was done on species with long development times (i.e.
planktotrophs). Ultimately, the goal in studying links between
life-history stages is to understand their long-term
consequences—individual longitudinal studies have important
implications for conservation efforts , predicting responses to climate
change , and can also better our understanding on the evolution of life
histories . Our literature map highlights how limited our understanding
of long-term theoretical and applied consequences of phenotypic links
is—improving culturing methods so we can make measurements at maturity
is an important first step in rectifying this problem.
Laboratory versus Field. Unsurprisingly, 12% of studies in the
dataset were conducted under field conditions, and of the field
experiments, less than 6% were individual longitudinal studies.
Conducting experiments in the field is important because tests in the
laboratory can sometimes yield conflicting results—for example if a
trade-off only exists in nature . The first and best examples of
field-based, individual longitudinal studies are in birds, primates and
other mammals—these studies are disproportionately represented in the
literature, reflecting both how rare and difficult generating
individual-based studies in the field is, as well as how useful they are
in answering ecological and evolutionary questions . Field experiments
will help reveal whether patterns, or links between stages, observed in
the laboratory, match patterns under natural conditions.
Taxonomic representation. For the 15 phyla in the dataset,
molluscs, echinoderms and arthropods make up ~70% of
species. Mollusca is the largest marine phylum with
~50,000 species, followed by arthropods and then
echinoderms . We found an overrepresentation of echinoderms—
Echinodermata is the third largest marine phylum but the second most
abundant in our map. The overrepresentation of echinoderms may suggest a
bias toward certain model species—five of the ten most common species
in the dataset were echinoderms: four sea urchins (Arbacia
punctulata , Paracentrotus lividus , Strongylocentrotus
droebachiensis , Strongylocentrotus purpuratus ) and one sand
dollar (Dendraster excentricus ). While model species, likeStrongylocentrotus purpuratus , Drosophila melanogaster orDanio rerio , are convenient and often economical, they do not
necessarily represent the consequences of links between life-history
stages across all taxa. The presence of links depends on species—for
example, significant genetic correlations between tadpole and adult
morphological traits were found for the anuran Hyla regilla , but
not Hyla cinerea or Rana sylvatica . To understand whether
patterns of links in the life history apply broadly across taxa, future
studies should use taxonomic groups that are insufficiently represented.
Summary. Our systematic map shows that, for over 100 years, the
studies of marine invertebrates have primarily collected data conducive
to characterising life histories, rather than understanding links
between stages. Studies following a single cohort are an important first
step for answering questions about development but when trying to
understand links across stages, cohort studies may lead to Simpson’s
Paradox, where the pattern across cohorts does not reflect the pattern
across individuals. The best strategy for avoiding Simpson’s Paradox is
to conduct individual longitudinal studies—those that follow
individuals through the entire life history, but these remain
exceedingly rare, accounting for just 1.7% of studies in our map.
Reviews in terrestrial systems also suggest that we move toward an
individual longitudinal approach when studying life histories , and
after systematically quantifying study types in the field using marine
invertebrates as a model system, we support those reviews. We
acknowledge and celebrate the tremendous progress in the field of
complex life cycles, but we hope that our map encourages future studies
to use an individual longitudinal approach to understand the ecological
and evolutionary significance of phenotypic links across life-history
stages.
Acknowledgements: We thank Annie Guillaume, Henry Wootton and
Victor Shelamoff for helping to collect data. We also thank Liz Morris
for editing the manuscript.