REVI EW AND

SYNTHESI S Phenotypic variation and selective mortality as major drivers

of recruitment variability in shes
Darren W. Johnson,
1
* Kirsten
Grorud-Colvert,
2
Su Sponaugle
3,2
and Brice X. Semmens
1
1
Marine Biology Research Division,
Scripps Institution of Oceanogra-
phy, UC San Diego, La Jolla, CA,
92023, USA
2
Department of Integrative Biology,
Oregon State University, 3029
Cordley Hall, Corvallis, Oregon,
97330, USA
3
Marine Biology and Fisheries,
Rosenstiel School of Marine and
Atmospheric Science, University of
Miami, 4600 Rickenbacker Cause-
way, Miami, Florida, 33149, USA
*Correspondence and present
address: Department of Biological
Sciences, California State University,
Long Beach. 1250 Bellower Blvd.,
Long Beach, CA, 90840, USA.
E-mail: darren.johnson@csulb.edu
Abstract
An individuals phenotype will usually inuence its probability of survival. However, when evalu-
ating the dynamics of populations, the role of selective mortality is not always clear. Not all mor-
tality is selective, patterns of selective mortality may vary, and it is often unknown how selective
mortality compares or interacts with other sources of mortality. As a result, there is seldom a
clear expectation for how changes in the phenotypic composition of populations will translate into
differences in average survival. We address these issues by evaluating how selective mortality
affects recruitment of sh populations. First, we provide a quantitative review of selective mortal-
ity. Our results show that most of the mortality during early life is selective, and that variation in
phenotypes can have large effects on survival. Next, we describe an analytical framework that
accounts for variation in selection, while also describing the amount of selective mortality experi-
enced by different cohorts recruiting to a single population. This framework is based on recon-
structing tness surfaces from phenotypic selection measurements, and can be employed for either
single or multiple traits. Finally, we show how this framework can be integrated with models of
density-dependent survival to improve our understanding of recruitment variability and popula-
tion dynamics.
Keywords
Density-dependent selection, tness surface, natural selection, population dynamics, stockrecruit
relationships.
Ecology Letters (2014) 17: 743755
INTRODUCTION
The dynamics of populations can be affected by both the
quantity and quality of the individuals within them. That is,
the demographic processes that drive the dynamics of popula-
tions are inuenced by both the number of individuals and
the phenotypes of those individuals. Classic theory has em-
phasised numerical effects such as density-dependent regula-
tion as the major, endogenous force driving the dynamics of
populations (reviewed by Murdoch 1994; Cappuccino & Price
1995). However, the phenotypic composition of a population
can also exert a strong inuence on population dynamics,
especially if the phenotypes under study are closely related to
demographic components of tness (reviewed by Gaillard
et al. 2000; Hairston et al. 2005; Schoener 2011). Despite
these observations, in practice it can be difcult to predict
how changes in the distribution of phenotypes within a popu-
lation will actually translate into variation in population
dynamics (reviewed by Saccheri & Hanski 2006; Kokko &
L opez-Sepulcre 2007; Metcalf & Pavard 2007). This is particu-
larly true for processes such as population replenishment,
which may depend on complex, non-linear relationships
among phenotype, mortality and density.
Although it has long been recognised that the phenotypic
composition of populations will inuence their dynamics, an
overall appreciation of the magnitude of these effects (espe-
cially relative to environmental factors as a source of variabil-
ity) has advanced more slowly (reviewed by Thompson 1998;
Benton et al. 2006; Kokko & L opez-Sepulcre 2007; Pelletier
et al. 2009). In part, this delay has been because classical
demographic analyses and models (in which individuals are
treated as identical) are simple and accessible, whereas the
quantitative tools for analysing phenotypic variation (and its
relative inuence on dynamics) require more data and have
taken time to develop (e.g. Lande 1976; Lande & Arnold
1983; Bjrnstad & Hansen 1994; Van Tienderen 2000;
Smallegange & Coulson 2013). A major advance in this eld
came when Hairston et al. (2005) presented a general frame-
work for disentangling the inuences of both phenotypic trait
change and environmental variation on population dynamics
(also see Ellner et al. 2011 for extensions of this approach). In
this framework, the partitioning of environmental and pheno-
typic contributions to population dynamics is accomplished
by analysing time-series observations of population-level
responses (e.g. population size), and average values of both
phenotypes and environmental variables of interest. This
framework has been applied to several empirical studies (e.g.
Ezard et al. 2009; also see examples in Hairston et al. 2005;
Ellner et al. 2011), and can be quite successful at illustrating
how phenotype change can affect dynamics. However, a
strong (and potentially limiting) assumption of the methods
proposed by Hairston and colleagues is that any effects of
changes in the distribution of phenotypes are a function of
changes in the mean value. This assumption may hold if the
2014 John Wiley & Sons Ltd/CNRS
Ecology Letters, (2014) 17: 743755 doi: 10.1111/ele.12273
relationships between phenotypes and population response
variables (e.g. per capita growth rate, survival, fecundity, etc.)
are linear (Ellner et al. 2011). However, if such relationships
are not linear, then through non-linear averaging (e.g. Ruel &
Ayres 1999) both the means and variances of phenotype dis-
tributions can play an important role in population dynamics,
and other approaches are needed. In this study, we present a
framework that can accommodate strong non-linearities in the
relationships between phenotypes and tness and thus can be
very useful in analysing how phenotypic variation can affect
population dynamics, even in the presence of strong density
dependence (another non-linear relationship). We apply this
framework to studies of selective mortality in sh populations
and use it to shed light on how variation in phenotypes may
drive variability in recruitment.
Replenishment of sh populations is notoriously variable.
In part, this is because most shes have life histories in which
numerous offspring are produced, but very few survive to
adulthood. A consequence of having a life history in which
early stages can be extremely abundant (often outnumbering
adults by several orders of magnitude) is that even small
changes in mortality during early life can have large effects on
recruitment (Houde 1987). Because seemingly small variations
in mortality easily can be responsible for order-of-magnitude
uctuations in recruitment, scientists have long been interested
in the characteristics of individuals that drive variation in
mortality during early life (e.g. Anderson 1988; Miller et al.
1988, Bailey & Houde 1989; Houde 2008).
The relationship between individual phenotype and relative
survival during early life can be examined through the lens of
phenotypic selection analysis (Lande & Arnold 1983). Pheno-
typic selection analysis has long been used to understand evo-
lutionary trajectories, but a main feature is that it separates
selection from inheritance. When such analyses are made
without information on heredity, they cannot be used to pre-
dict evolution. However, they may still be used to understand
selection as a within-generation, demographic process.
The last few decades have seen a rise of studies examining
how the relative survival of shes is inuenced by phenotypic
characteristics. The realisation that sh otoliths (accretions of
calcium carbonate around protein matrices in the inner ear)
can carry a permanent record of traits related to size, growth
rate, and condition has enabled studies of selective mortality
and yielded important insight into why certain individuals sur-
vive and others do not (Sponaugle 2010). Recent reviews of
this eld indicate that selection (i.e. the change in the pheno-
type distribution that is generated by differential mortality) is
typically very strong during early life phases of shes (Sogard
1997; Perez & Munch 2010). Both of these reviews noted a
substantial amount of variability in selection, although neither
study examined selective mortality at the scale of the popula-
tion, and neither study explored how variation in selection
may affect population dynamics. Selection during early life
can be summarised using selection coefcients, but it is impor-
tant to keep in mind that survival during early life is only a
component of tness. From an evolutionary viewpoint, one
might expect early mortality to be strongly selective with
respect to traits such as size and growth (which are commonly
measured traits in this eld). Mothers may trade offspring size
for offspring number, and the maximisation of tness may
come at the expense of offspring survival (Vance 1973; Smith
& Fretwell 1974). As a result, the relationship between early
life traits and a more complete measure of tness (e.g. lifetime
reproductive success of mothers) may indicate stabilising,
rather than directional, selection because reproductive success
is a combination of both the number of offspring and their
survival (e.g. Smith & Fretwell 1974; see Einum & Fleming
2000; Johnson et al. 2010; for empirical examples in shes).
A consequence of this phenomenon is that even though early
life-history traits may be evolutionarily stable, there can still
be very large differences in the relative probability of survival
of individuals during early life (as evidenced by many empiri-
cal studies; Sogard 1997; Perez & Munch 2010).
That selection is widespread and often strong provides evi-
dence that an individuals phenotype can strongly inuence its
relative probability of survival. However, at the level of the
population, understanding how phenotypic variability affects
recruitment is much more complicated. First, it can be unclear
whether the amount of selective mortality incurred is substan-
tial enough to be important to the dynamics of populations.
The amount of selective mortality that a population or a
cohort (i.e. a group of similarly aged individuals) experiences,
and how that compares to total mortality, is not often quanti-
ed. Second, selection may be highly variable. Even when one
considers selection on a single trait in a focal population,
measurements often vary substantially (e.g. Meekan & Fortier
1996; Good et al. 2001; Rankin & Sponaugle 2011), making it
difcult to discern any general patterns. Finally, it remains
unclear how selective mortality compares or interacts with
density-dependent mortality a major factor inuencing early
survival and recruitment (reviewed by Myers & Cadigan 1993;
Rose et al. 2001; Hixon & Webster 2002). Box 1 outlines a
general approach to quantifying selective mortality and to
partitioning population-level mortality into selective and non-
selective components.
To understand how phenotypic variation affects mortality
within cohorts and therefore recruitment to populations, we
need to study selection within a quantitative, analytical frame-
work. Here, we review empirical studies of selection in shes
as a rst step towards evaluating the overall importance of
selective mortality to recruitment. Next, we describe an ana-
lytical framework that accounts for variation in selection,
while also describing the amount of selective mortality experi-
enced by cohorts. This framework is based on empirical
reconstruction of tness surfaces from selection measure-
ments, and can be employed for either single, or multiple
traits. Finally, we show how this framework can be integrated
with models of density-dependent survival to improve our
understanding of recruitment variability.
SELECTION, DEMOGRAPHIC COSTS AND
RECRUITMENT VARIABILITY IN FISHES
Selection implies a demographic cost to the population. When
phenotype distributions change through differential mortality,
stronger selection implies greater mortality overall. Demo-
graphic costs of selection can therefore be important in the
context of recruitment where dynamics are driven by variation
2014 John Wiley & Sons Ltd/CNRS
744 D. W. Johnson et al. Review and Synthesis
in both cohort size and cohort mortality. All else being equal,
cohorts that experience stronger selection must incur greater
mortality (i.e. greater costs), and if cohorts that recruit to a
population vary in the degree of selection (and selective mor-
tality), then selective mortality may be an important source of
variability in total mortality, and thus variability in recruit-
ment (Box 1).
As a rst step towards evaluating variability in selective
mortality and its potential role in generating recruitment vari-
ability, we compiled published estimates of selection on early
life traits in shes. For many shes, synchrony in reproduction
and/or settlement from the plankton produces discrete cohorts
that settle at approximately the same age. Selection measure-
ments are typically made within cohorts and selection measure-
ments can be used to infer mortality (Box 1). To evaluate how
selective mortality affects recruitment to particular popula-
tions, we need to examine variability in selective mortality
among cohorts because it is among-cohort variation in mortal-
ity that contributes to recruitment variability. In our literature
search, we considered only those studies that estimated selec-
tion on the same focal trait(s) for two or more separate
cohorts. Our search yielded a total of 136 selection estimates
for 33 species (Table S1, also see Appendix S1 in Supporting
Information). Although very few studies of selection have
actual estimates of total mortality, we were able to derive esti-
mates of selective mortality from measurements of selection.
Selection is typically measured by the selection differential,
i.e. the mean phenotypic value of the population after selection
minus the mean before selection (Falconer & Mackay 1996).
For each cohort, we estimated the amount of selective mortality
that would be necessary to generate the observed selection dif-
ferential, given the assumption that before selection, traits were
normally distributed with the observed means and variances.
For this analysis, selection was assumed to be generated by
truncation mortality (e.g. all individuals with phenotypic values
above a certain threshold (z
t
) survived and all below died this
pattern could be reversed if smaller phenotypes were favoured).
For example, f
z
= 0 for z > z
t
and f
z
= for z z
t
. To calculate
truncation mortality, we used a simple optimisation routine to
nd the truncation point on a standard normal distribution that
would produce a truncated distribution of survivors with a
mean value that would produce the same standardised selection
differential as the one observed for each cohort. We then calcu-
lated selective mortality as 1 minus the integral of the truncated
distribution. We chose truncation as the functional form of
selection because it is the most efcient form of selection, and
Box 1 Components of mortality
Consider a population in which individuals risk mortality from multiple sources, some of which are selective with respect to
phenotype, and others that are not. Let n
z,t
describe the number of individuals of phenotype z at time t. This distribution will
change through time as individuals are removed from the population through both selective and non-selective mortality. The
rate of selective mortality, f
z
, is a function of phenotype and the rate of non-selective mortality, a, is a constant. There-
fore,
@n
z;t
@t
an
z;t
f
z
n
z;t
:
From the previous expression, the distribution of phenotypes at time t + 1 can be obtained: n
z;t1
n
z;t
e
af
z
and population size (total abundance) at time t + 1 is then N
t1

R
n
z;t1
dz e
a
R
e
f
z
n
z;t
dz:
Factoring in the distribution of phenotypes at time t yields N
t1
e
a
R
e
fz
nz;tdz
R
n
z;t
dz
R
n
z;t
dz;
which can be expressed as: N
t1
e
a
R
e
fz
n
z;t
dz
Nt
R
N
t
;
or equivalently N
t1
e
a
W
z
N
t
;
where W
z
selective survival
R
e
fz
n
z;t
dz
Nt
:
At the level of the population (or cohort, or group), mortality can be separated into two components: selective mortality (1-
W
z
), and non-selective mortality W
z
1 e
a
.Total mortality (M
TOT
) is 1 e
a
W
z
and may range from 0 to 1. From these
relationships we can conclude that when the selective component of mortality is large, the non-selective component must be
small. We can also conclude that because selective mortality is a component of total mortality, variation in selective mortality
among cohorts will translate to variation in the total amount of mortality that cohorts experience. This translation will be direct
if the rate of non-selective mortality (a) is constant among cohorts (or at least random with respect to selective mortality).
In many cases, patterns of selection (i.e. changes in the distributions of phenotypic values) are driven by selective mortality.
Even if mortality is not measured directly, the amount of selective mortality a population experiences can be inferred from
selection measurements. Empirical measurements of selection often focus on calculating the selection differential, i.e. the mean
phenotypic value after selection minus the mean before selection (Falconer & Mackay 1996). The selection differential (S) can
also be expressed in terms of the (normalised) distribution of phenotypes before selection and the selective mortality function.
Specically,S
R
znz;te
fz
dz
R
nz;t e
fz
dz
z:
If the selection differentials and phenotype distributions are known, and if a simple functional form (e.g. truncation selection)
is chosen to describe the rate of selective mortality, then the parameters dening f
z
can be solved for and the amount of selec-
tive mortality can be calculated as described above.
2014 John Wiley & Sons Ltd/CNRS
Review and Synthesis Selective mortality and recruitment 745
therefore provides the most conservative estimate of selective
mortality (Van Valen 1965). However, other functional forms
of selection are possible. To examine how sensitive the conclu-
sions of this analysis would be to choice of functional form, we
repeated this analysis assuming that selection can be described
by a less efcient, Gaussian function (Appendix S1). We recog-
nise that the functional form of selection may vary among
cohorts, but choosing a single functional form to describe selec-
tion allows for a standardised comparison among cohorts, spe-
cies, etc. This analysis is therefore meant as a broad-stroke
summary of variation in selective mortality.
On average, the amount of selective mortality experienced
by cohorts of sh during recruitment was substantial (the
median of the within-species average amount of selective mor-
tality was 0.52; Fig. 1a). Noting that truncation mortality pro-
vides a conservatively low estimate of selective mortality, and
that total mortality is less than 1, these results suggest that
much of the mortality during early life is selective mortality
(i.e. median, within-species average non-selective mortality
< 0.48). If selection is assumed to follow a modied Gaussian
form, then selective mortality was expected to be greater
(median, within-species average = 0.79, implying non-selective
mortality < 0.21). Importantly, the range of selective mortality
values within species (i.e. the difference between the highest
and lowest values) also tended to be large, and did not differ
much based on choice of functional form. For both trunca-
tion and modied Gaussian mortality, median, within-species
range of selective mortality was 0.40 (Fig. 1b). Again, these
estimates may be conservative because the analyses assume no
variation in the functional form of selection. Although these
data represent rough estimates, they do suggest that variabil-
ity in selective mortality can lead to substantial variation in
total survival. This, in turn, suggests that selective mortality
can be a large source of variation in recruitment.
WHY DO SELECTION MEASUREMENTS VARY?
Measurements of selection (e.g. selection differentials) can vary
across cohorts for multiple reasons. First, we need to recognise
the effects of measurement error, which can cause apparent
differences in the strength (and even direction) of selection
(e.g. Mitchell-Olds & Shaw 1987; Siepielski et al. 2009; Morris-
sey & Hadeld 2012). Inference about selection always
involves sampling, and often involves comparing two samples
(one before and one after selection). Sampling error will inate
the apparent variability in selection when comparing among
cohorts. Strictly speaking, sampling error cannot be avoided,
but large sample sizes will help minimise the effects of sam-
pling error. A second form of measurement error stems from
the fact that survival is often inuenced by multiple, correlated
traits. Even if selection on a particular trait of interest remains
constant across cohorts, differences in selection on other, cor-
related traits, and/or differences in the correlation between
traits can cause selection differentials to vary. Analysing selec-
tion within a multivariate framework allows one to measure
the direct effects of selection on each trait and can greatly min-
imise the variability associated with correlation among traits
(Lande & Arnold 1983; see Johnson et al. 2012 for applica-
tions to before- and after-selection samples).
Real differences in selective mortality across cohorts can be
caused by two phenomena. First, the tness surface (in the
case of recruitment, the relationship between phenotypic value
and expected survival) may vary among cohorts. Differences
in the biotic and/or abiotic environment may change the
shape, location or form of the tness surface. There are many
well-known examples where environmental changes clearly
alter the tness surface. For example, sh that are experimen-
tally separated from major predators may experience changes
in selection on traits such as colouration (e.g. Endler 1980),
defensive morphology (e.g. Marchinko 2009) and maturation
time (e.g. Reznick & Bryga 1987). In other cases, tness sur-
faces may change in response to the number of competitors,
and selection may thus be density dependent (Einum et al.
2008). However, in many ecological scenarios (e.g. different
cohorts of larvae settling to the same habitat over time with
no obvious changes in the environment) tness surfaces may
change little, if at all.
A second reason why selection may vary is that the distri-
bution of phenotypes often varies across cohorts. Different
cohorts may have developed under dissimilar environmental
conditions and/or originated from genetically different source
populations, leading to variation in the distributions of phe-
notypes. Such variation in phenotype distributions can be a
major source of systematic variation in selection (e.g. Endler
(a)
(b)
Figure 1 Estimated amount of selective mortality experienced by cohorts
of larval and juvenile sh (n = 34 populations, representing 33 species).
(a) Average amount of selective mortality, and (b) variability in selective
mortality within each population. See Appendix S1 for data sources and
additional details regarding the analyses.
2014 John Wiley & Sons Ltd/CNRS
746 D. W. Johnson et al. Review and Synthesis
1986; Weis et al. 1992; Steele et al. 2011). Central to this
phenomenon is the fact that tness surfaces are typically
non-linear. For example, expected survival is bounded
between 0 and 1, so relationships between phenotype and rel-
ative survival can be strongly non-linear. Moreover, it is fre-
quently observed that optimal survival often occurs at
intermediate, rather than extreme phenotypes (Janzen &
Stern 1998). On a non-linear tness surface that remains con-
stant, cohorts with different distributions of phenotypes will
sample different areas of the tness surface, resulting in dif-
ferences in the magnitude, and sometimes even the direction
of selection (Fig. 2).
Fitness surfaces are not necessarily constant across cohorts,
as changes in the environment may cause tness surfaces to
vary. However, we believe that an essentially constant tness
surface is not necessarily a rare scenario. Rigorously evaluat-
ing whether tness surfaces actually differ in space and time
requires multiple estimates of selection and an appropriate
null model for selection variation. When estimates of tness
surfaces (or summaries such as selection coefcients) vary, it
may be tempting to conclude that the underlying tness sur-
faces are different. However, we believe that such differences
should be considered apparent differences in tness surfaces
until the effects of sampling different regions of a non-linear,
but constant tness surface can be ruled out.
In the sections below, we discuss how a constant tness sur-
face may provide a parsimonious model to explain variation
in selection. When data from multiple cohorts are available,
and their distributions of phenotypes vary, systematic varia-
tion in selection measurements can provide evidence of
whether the tness surface can be treated as constant across
cohorts. Because cohorts of sh can vary substantially with
respect to the distribution of their phenotypes (in our review,
median CV of cohort means = 7.6%, median CV of within-
cohort standard deviations = 23.0%), the effects of such
variation on selective mortality and recruitment may be large.
We also discuss how the assumption of a constant tness sur-
face and the techniques described below may be appropriate
for other taxa and ecological scenarios (see Discussion and
Appendix S2 in Supporting Information).
RECONSTRUCTING FITNESS SURFACES TO
EVALUATE RECRUITMENT
If tness surfaces are constant and non-linear, then cohorts
that differ with respect to their distribution of phenotypes will
experience different patterns of selection. However, it is often
the case that tness surfaces are unknown (especially across a
broad range of phenotypic values). Rather, investigators typi-
cally know the means and variances of trait values before and
after a period of selective mortality, and can therefore
estimate selection. When multiple estimates of selection are
available, one can look for a systematic relationship between
trait distributions and selection estimates as evidence of a con-
stant tness surface. If the tness surface can be assumed to
be reasonably constant, then one can use selection estimates
to reconstruct the tness surface over a broad range of pheno-
typic values. Describing the tness surface provides a frame-
work for inferring differences in selective mortality among
cohorts. This framework can be extremely useful in that it (1)
offers an explanation for differences in observed measures of
selection, and (2) describes differences in relative survival
among cohorts, even when direct measures of mortality are
unavailable.
To illustrate this approach, we examined variation in selec-
tion on pelagic larval duration (PLD) among cohorts of a
common, demersal blenny (Lipophrys trigloides). Data come
from Macpherson & Raventos (2005) study of post-settle-
ment, selective mortality. These authors measured selective
mortality on PLD for eight different cohorts. Samples of
recent settlers were collected and PLD was measured from ot-
oliths. Juveniles of the same cohorts were collected ~45 days
later. Distributions of PLD values were compared between
initial settlers and surviving juveniles in a standard, before-
after approach. Note that Macpherson & Raventos (2005)
also measured selection on other traits (including size at
hatching and size at settlement). Here, we concentrate on a
single trait (PLD) to illustrate the analytical approach in the
univariate case. A multivariate approach, which explicitly
considers mortality that is selective with respect to multiple
traits, is described in a subsequent section.
(a) (b) (c)
Figure 2 Variation in phenotype distributions as a cause of variation in selection measurements. If tness surfaces are non-linear and constant across cohorts,
then selection differentials, S, will depend on the distributions of phenotypes. (a) When the distribution of phenotypes is centred at the phenotypic optimum
(the peak of the tness surface), there is no directional selection (S = 0). (b) When phenotypes are, on average, smaller, there is directional selection
favouring larger individuals. (c) When mean phenotype is the same as in (b), but the variance is greater, much more of the phenotype distribution is far out
on the left tail where survival is very low. There is a correspondingly greater shift in the mean, and a greater selection differential. The same principles apply
to the multivariate case, except that selection differentials may also vary because of differences in the distributions of other, correlated traits.
2014 John Wiley & Sons Ltd/CNRS
Review and Synthesis Selective mortality and recruitment 747
Selection differentials associated with PLD tended to be
negative (mean = 1.01, range = 2.37 to 0.46 when standar-
dised to a common measure of variance) suggesting that
within cohorts, sh that had shorter PLDs tended to survive
better (shorter PLD is likely related to faster growth and/or
better condition). Among cohorts, the magnitude of selection
changed systematically with average phenotypic value
(Fig. 3a). Cohorts that had shorter average PLDs experienced
weaker selection, and therefore less selective mortality.
Selection differentials describe the slope of the tness sur-
face at the cohort mean (Phillips & Arnold 1989). If the selec-
tion differentials change linearly with mean phenotypic value
(and variances are similar among cohorts), it suggests that
over a broad range of phenotypes the tness surface (i.e. the
relationship between phenotypic value and expected tness)
may be reasonably described by a Gaussian function. Dening
the tness function (W
z
) as Gaussian, then
W
z
e
a
zh
2
zx
2
; 1
where h is the optimal phenotypic value, x indicates the width
of the curve describing tness and a species the magnitude
of non-selective mortality. A Gaussian tness function has the
desirable property that tness cannot be negative. Moreover,
the Gaussian function is somewhat exible. Depending on
parameter values and the phenotypic range of interest, a
Gaussian function can describe several forms of selection (e.g.
concave up, approximately linear, or concave down). If the
distribution of trait values before selection, p
z
, is normal with
mean z and variance r
2
, r selection differential, S, can be
calculated as
S
zx
2
hr
2

x
2
r
2

Z; 2
(Lande 1981). Note that the value of selection differentials
will change with both the mean and variance of phenotypes
before selection.
If selection can be measured for multiple cohorts, then one
can estimate parameters of the underlying tness surface by
nding the parameters of eqn 2 that are most likely to have
produced the observed values of S, given values of z and r
2
.
The degree of t between predicted and observed values of S
can provide a heuristic indication of how well selection can be
described by a constant tness surface. Once the tness sur-
face (W
z
) is estimated, the mean tness (survival) of a cohort
can also be estimated as p
z
W
z
dz, where p
z
is the phenotype
distribution specied by the mean and variance of phenotypic
values before selection.
We used maximum likelihood to t a non-linear model
(eqn 2) to Macpherson & Raventos (2005) data on selection
differentials on PLD. Our likelihood function was specied by
assuming that the residual variation of the selection differentials
was normally distributed with equal variance across observa-
tions. Mean values were specied by eqn 2, and variance was
estimated from the data. We used the optim function in R
(R Development Core Team 2013) and a Nelder-Mead
non-linear optimisation algorithm to nd the parameter
values of eqn 2 that were most likely to have produced
the observed selection differentials. As a measure of explana-
tory power, we used a pseudo r
2
value, dened as
1
P
obs: pred:
2
=
P
obs: mean
2
. Note that although a
value of 1 is possible only when there is absolutely no measure-
ment error in observed values S, this statistic provides a useful
approximation for the explanatory power of non-linear models.
A Gaussian surface did a reasonable job of describing
variation in selection differentials (pseudo r
2
= 0.61). This esti-
mate of the tness surface suggested that shorter PLDs were
favoured, with an optimum suggested to be somewhere in the
vicinity of 2 SD below the overall, among-cohort mean PLD
(Fig. 3b). One can estimate selective mortality for each cohort
by calculating the area of overlap between the distribution of
phenotypes and the tness surface. This estimates the mini-
mum amount of mortality a cohort experiences, since it does
not include non-selective mortality (nor does it include mor-
tality that is selective, but independent of the focal trait).
Estimates of selective mortality associated with PLD ranged
(a)
(b)
Figure 3 (a) Variation in selection on pelagic larval duration (PLD) in a
demersal blenny (Lipophyrs trigloides). Cohorts with shorter average
PLDs experienced weaker selection (PLD values are centred and scaled to
the average, within-cohort SD). Data from Macpherson & Raventos
(2005). (b) Estimated tness surface relating PLD to survival. The degree
of mismatch between the distribution of phenotypes (dashed lines) and
the tness surface (solid line) determines the amount of selective
mortality. For cohort 1 (white histogram), only those individuals in the
lower tail of the distribution have an appreciable probability of survival.
This results in a large shift in mean value (S = 2.37) and high selective
mortality ( 0.96). For cohort 8 (grey histogram) the mean is near the
estimated peak of tness curve, suggesting little directional selection.
Moreover, this distribution overlaps a region of high tness, suggesting
that selective mortality is low ( 0.35).
2014 John Wiley & Sons Ltd/CNRS
748 D. W. Johnson et al. Review and Synthesis
from 0.35 to 0.96. Assuming non-selective mortality is similar
across cohorts, these are large differences in relative survival.
A multivariate example
When estimates of means, variances, covariances and selection
differentials are available for multiple traits and multiple
cohorts, a similar procedure can be used to estimate a multi-
variate tness surface. Although multivariate tness surfaces
can be more difcult to display, they are likely to be more
accurate because selection gradients are likely to be more
accurate than selection differentials (Lande & Arnold 1983).
Also, explicitly accounting for trait covariances and correla-
tional selection will provide a more accurate accounting of
selective mortality.
To illustrate how selection measurements can be used to
reconstruct multivariate tness surfaces over a broad range of
phenotypic values, we used data from a study of selective
mortality on early life-history traits in a reef-associated wrasse
(Thalassoma bifasciatum; Grorud-Colvert & Sponaugle 2011).
Within this dataset, measurements of selection were made for
eight cohorts of sh settling to similar reef habitats in the
Florida Keys, USA. Larvae of this species settle and bury into
sand and rubble habitat for 35 days while they undergo
metamorphosis. The before-selection sample represents sh
that were captured immediately after emergence (i.e. sh
whose ages were 04 days post emergence). The after-selection
sample represents sh of the same cohort that were captured
as surviving juveniles (ages > 9 days post emergence). For this
example we analysed selective mortality on larval growth rate
(estimated from width of otolith increments during the larval
stage), and width of the metamorphic band deposited in the
otolith during metamorphosis (an indicator of settlement con-
dition and energy reserves; Hamilton 2008).
As a rst step in evaluating whether variation in multivari-
ate selection can be explained by phenotypic variation on a
constant, multivariate surface, we examined relationships
between distributions of trait values and strength of selection.
For each cohort, we calculated selection gradients on both
larval growth and condition using the procedures outlined by
Johnson et al. (2012). Briey, for each cohort we used the
differences in means before and after selection to calculate
selection differentials, and then multiplied this vector by the
inverse of the observed variancecovariance matrix to convert
selection differentials to selection gradients. Selection gradi-
ents measure direct selection on each trait and provide a mea-
sure of the slope of the tness surface along the direction of
the focal phenotype (Phillips & Arnold 1989). These slope
estimates are averaged across the observed distribution of
phenotypes, and if the tness surface is non-linear, selection
gradients will depend on trait variances. However, examining
relationships between selection gradients and mean trait val-
ues can still provide a useful, rst look at the tness surface.
The results of such exploratory procedures can then be used
to inform subsequent analyses.
For condition, the selection gradients varied strongly with
mean phenotypic value (Fig. 4). These data suggest a tness
surface that is constant and that becomes less steep as condition
increases, but levels out (i.e. the slope approaches zero) at
~0.5 SD above the mean. Selection gradients varied much less
for larval growth (Fig. 4b) and many of the values were near
zero, suggesting a low slope in the vicinity of the observed mean
values. Variances in the after-selection samples tended to be
smaller than those in the before-selection samples (mean values
of the variance ratios were 0.74 for condition, 0.82 for larval
growth), suggesting a concave-down tness surface. Taken
together, these data suggest that a Gaussian function may be a
reasonable model for the tness surface (Lande 1981).
Assuming that tness can be described as a multivariate,
Gaussian function of phenotypic values then
W
z
exp a
1
2
z h
T
1z h

; 3
where the vector h indicates the location of the phenotypic opti-
mum, the matrix x describes the dispersion of tness values
about the optimum and a describes non-selective mortality.
Assuming that the distribution of phenotypes before selection
can be described as multivariate normal with means z and
covariance matrix P, then the distribution of phenotypes after
selection is also a multivariate Gaussian distribution with a vec-
tor of means, z

, and a covariance matrix, P*, described as

z

x P
1
xz P 4a
(a)
(c)
(b)
Figure 4 (a, b) Variation in selection on larval condition and growth in
the bluehead wrasse (Thalassoma bifasciatum). Selection gradients
estimate direct selection on each trait and trait values are centred and
scaled to the average, within-cohort SD. The strength of directional
selection on condition decreased with the mean value. Directional
selection on larval growth was much weaker. Numbers above each point
indicate cohort identity and are labelled as in the original study (cohorts.
Data from Grorud-Colvert & Sponaugle (2011). (c) Estimated tness
surface relating larval growth and condition to survival. Contours
represent lines of equal tness (survival probability) along a multivariate
Gaussian surface. Points indicate the bivariate means for each cohort.
2014 John Wiley & Sons Ltd/CNRS
Review and Synthesis Selective mortality and recruitment 749
P

x P
1
xP: 4b
Note that in the multivariate case, the values of the selec-
tion differentials z

z can change with the distribution of

the focal phenotype and with the distribution of other, corre-
lated traits. In other words, selection differentials will depend
on the means and covariances of the traits before selection.
To t a Gaussian function to the data on selection in blue-
head wrasse, we estimated the values of h and x that were
most likely to have produced the observed changes in the
means and (co)variances of phenotypes for each cohort. Our
likelihood function was specied by assuming that for each
cohort the observed means after selection were distributed as
multivariate Gaussian. Expected values for the means after
selection were described by eqn 4a. The dispersion of these
means was described by the expected covariance matrix after
selection (eqn 4b) divided by the number of individuals in
the after-selection sample for each cohort. Observed covari-
ances after selection were assumed to follow a Wishart distri-
bution with the degrees of freedom specied as the number
of individuals in the after-selection sample minus one (Press
2012). The joint likelihood was calculated as the product of
likelihoods for the means and the covariances, and the prod-
uct of this quantity was taken across all cohorts. We used
the optim package in R (R Development Core Team 2013)
and a Nelder-Mead algorithm to obtain maximum likelihood
estimates of h and x.
Modelling the multivariate tness surface as a constant,
Gaussian function explained much of the observed variation
in selection. When considering the entire data set of tted val-
ues (2 after-selection means + 3 elements of an after-selection
covariance matrix for each of eight cohorts = 40 tted values),
the pseudo r
2
for the relationship between predicted and
observed values was 0.57. The estimated tness surface indi-
cates that there was strong selection favouring faster larval
growth and greater condition (Fig. 4c). The data also suggest
selection for a positive combination of these traits. The tness
peak in the upper right quadrant suggests that individuals that
were in good condition and grew fast were individuals that
had especially high survival probabilities.
In addition to explaining variation in selection measure-
ments, by reconstructing a tness surface, we can estimate dif-
ferences in relative survival rates. The amount of selective
mortality a cohort experiences can be estimated by how much
the distribution of phenotypes (in the before-selection sample)
overlaps with the tness surface. Specically, selective mortal-
ity can be calculated by integrating the product of the multi-
variate density function describing the distribution of
phenotypes, p
z1,z2
, and the multivariate tness surface, W
z1,z2.
That is, selective mortality = 1
R R
p
z1z2
W
z1z2
dz
1
dz
2
. For
example, cohort 4 has a mean that is near the optimum of the
tness surface (Fig. 4c). This cohort is expected to have
relatively low selective mortality (0.61), whereas cohort 10 is
centred in an area of low tness and is expected to have high
selective mortality (0.84). The amount of overlap, and
therefore the average mortality within a cohort also depends
on the (co)variances of the traits involved. For these data,
estimated (selective) mortality within cohorts ranged from
0.38 to 0.84. Similar to our univariate example, these data
suggest that under some circumstances tness surfaces may be
reasonably constant and that variation in phenotypes can
cause substantial variation in survival and recruitment.
DENSITY DEPENDENCE, SELECTIVE MORTALITY AND
RECRUITMENT
Although for many shes, post-settlement mortality is strongly
selective (reviews by Sogard 1997; Perez & Munch 2010), post-
settlement mortality may also depend strongly on density
(reviews by Myers & Cadigan 1993; Rose et al. 2001; Hixon &
Webster 2002; Osenberg et al. 2002). For example, high densi-
ties of sh within a habitat may result in increased competition
among individuals and/or an increased response by predators,
which can lead to greater mortality rates (reviewed by Hixon &
Jones 2005). Because survival may be strongly inuenced by
both density and phenotype, it is useful to consider how these
attributes combine to inuence recruitment.
Simple, density-dependent models of recruitment [e.g.
Beverton & Holt (1957) and Ricker (1954) models of stock
recruitment relationships] capture the basic property of regu-
lation, but typically provide a poor t to real data (e.g. Iles
1994; Myers 2001). A limitation of such models may be that
they treat the underlying relationship between density and
mortality as constant. Recent studies suggest that density-
dependent recruitment is a complex process in which the
strength of density dependence may change with several fac-
tors, including characteristics of individuals (Shima et al.
2006; Johnson 2008). Given the strong and pervasive effects
of selective mortality during larval and juvenile phases
(Fig. 1), we believe it would be useful to consider models of
recruitment where an individuals probability of surviving
depends on both phenotype and density.
To illustrate how density and phenotype may jointly affect
recruitment, we consider a population where selection has
been well studied and recruitment is strongly regulated by
density-dependent mortality. The data describe recruitment of
steelhead trout (Oncorhyncus mykiss) in Snow Creek, Wash-
ington, USA (Seamons et al. 2007). First, we evaluated den-
sity dependence in recruitment by examining the relationship
between number of spawning adults and number of returning
offspring (sampled when they returned to spawn; Fig. 5).
These data, like many stockrecruitment curves, illustrate two
points: (1) the presence of strong density dependence, and (2)
relatively poor explanatory power (pseudo r
2
= 0.16).
Seamons et al. (2007) also measured selection on adult body
size. By tagging, measuring and sampling the tissue of virtually
all returning adult sh, the authors were able to use genetic par-
entage analysis to count how many returning offspring each
adult sh produced. The relationship between adult body size
and lifetime reproductive success provides a measure of the
strength of selection (Lande & Arnold 1983). Here, we analysed
variation in selection on male body size. Note that although
this example focuses on traits of adults (rather than offspring,
as in our previous examples) and measures recruitment as the
number of returning adults (rather than juveniles), the princi-
ples are entirely the same. Moreover, one of the reasons male
body size affects recruitment in salmonids may be because of
correlations between adult size and offspring size and perfor-
2014 John Wiley & Sons Ltd/CNRS
750 D. W. Johnson et al. Review and Synthesis
mance (Heath et al. 1999; Smoker et al. 2000). Because the
within-cohort variance differed substantially among cohorts,
we plotted the relationship between selection differentials and
both the cohort mean and variance (Fig. 6). Note that for some
of the cohorts in the original study, sample sizes to estimate
selection were very small. To avoid imprecision associated with
small samples, we restricted this analysis to selection estimates
from cohorts with n > 10. Although taken individually, these
sample sizes are small, our analyses focused on variation among
selection measurements across the 15 separate cohorts. Selec-
tion differentials changed substantially with both mean and
variance in phenotypic values, suggesting a non-linear tness
surface. Again, using maximum likelihood, we t eqn 2 to the
selection differentials as described above. A Gaussian tness
surface provided a good t to the selection data (pseudo r
2
for
the relationship between predicted and observed selection dif-
ferentials was 0.56, n = 15).
The data for selection on body size suggest that phenotypic
variation and selection on a constant tness surface can lead to
substantial variation in relative survival rates. But do these
inferences hold true when we look at more direct estimates of
survival, knowing that density dependence is strong? To evalu-
ate this, we can compare a simple, density-dependent model of
recruitment to a model in which individual survival probability
may be affected by both phenotype and density. To describe
density-dependent recruitment, we use a Ricker model:
N
R
N
S
e
abN
S
; 5
where N
R
is the number of recruits, N
S
is the number of
spawners, a describes the rate of offspring production (a com-
bination of fecundity and non-selective, density-independent
mortality) and b describes the rate of density-dependent mor-
tality. This model of density-dependent recruitment is appro-
priate for many salmonids because a strong mechanism of
density dependence results from greater disturbance of nests
and subsequent egg mortality when spawners are abundant
(Ricker 1954; McNeil 1964; Fukushima et al. 1998). However,
survival during later stages (especially juveniles) can depend
on body size (which is linked to parental body size; Heath
et al. 1999; Smoker et al. 2000; Carlson & Seamons 2008).
Following a similar procedure as in Box 1., the change in the
number of individuals (and distribution of phenotypes) over
time can be described as an outcome of three processes. Spe-
cically,
@n
z;t
@t
n
z;t
a bN
S
f
z
;
where a, b and N
S
are as in the density-dependent model, and
f
z
is a function describing the rate of selective mortality. The
distribution of phenotypes at time t + 1 is
n
z;t1
n
z;t
e
abN
S
f
z
and total abundance at time t + 1 is
N
t1
N
R
e
abNS
Z
n
z;t
e
fz
dz:
If body sizes are normally distributed within each cohort,
then n
z,t
can be described as the product of the number of
spawners (N
S
) and a normal probability density function (p
z
).
Dening f
z
as a scaled quadratic function (f
z
= (z h)
2
/2x
2
)
yields a Gaussian tness surface and integrating the former
expression yields our model for recruitment:
Figure 6 Relationship between observed selection differentials and the
means and variances of adult male body length for spawning cohorts of
steelhead trout. Mean values were standardised as deviations from the
grand mean, divided by the square root of the average, within-cohort
variance. Variances were standardised by dividing within-cohort variances
by the average variance. Response surface illustrates the expected value of
selection differentials based on the best-t, Gaussian tness surface.
Original data from Seamons et al. (2007).
Figure 5 Relationship between spawning stock abundance (number of
male adults) and the number of recruits for steelhead trout (Oncorhynchus
mykiss) in Snow Creek, Washington, USA over 19 years. Recruitment is
dened as the number of offspring (both sexes) that returned to spawn as
adults. Solid line represents t of a Ricker recruitment model. Data from
Seamons et al. (2007).
2014 John Wiley & Sons Ltd/CNRS
Review and Synthesis Selective mortality and recruitment 751
N
R

xN
S

x
2
r
2
p e

zh
2
2x
2
r
2
e
abNS
; 6
where h is the optimal phenotypic value, x indicates the width
of the curve describing tness, and z and r
2
are the mean and
variance of the cohort before selection. Other symbols are as
in eqn 5. Note that in this model, the function describing the
rate of selective mortality was not affected by density. This is
because in this system we expect the main mechanism of den-
sity dependence (egg mortality because of nest site disturbance
at high spawner density) to be largely independent of the
main source of selective mortality (size-selective predation
during the juvenile phase; Ward et al. 1989), which is trace-
able in our model due to the correlation between size of off-
spring and the size of male parents in salmonid populations
(Heath et al. 1999; Smoker et al. 2000; Carlson & Seamons
2008). However, if selection is expected to depend on density
(or any other measurable environmental factor), it is straight-
forward to incorporate these effects into f
z
(e.g. by modelling
selective mortality as a function of both phenotype and den-
sity; Appendix S2).
We t both the density-dependent model (eqn 5) and the
combined phenotype- and density-dependent model (eqn 6) to
the observed recruitment values. Our likelihood functions
were specied by assuming that the observed estimates of
recruitment were Poisson distributed with mean values
specied by either eqn 5 or eqn 6. In each case we used the
optim function in R (R Development Core Team 2013) and a
Nelder-Mead algorithm to nd the parameter values that were
most likely to have produced the observed pattern of recruit-
ment. Fitting both models to the data suggested that the
phenotype- and density-dependent model ts better
(AICc = 4.5), and that adding phenotypic variation as a pre-
dictor more than doubled the explanatory power of the
stockrecruit relationship (pseudo r
2
= 0.39). These results
suggest that even in a strongly density-regulated system, phe-
notypic variation and selective mortality can be an important
source of variation in survival and recruitment (Fig. 7). These
results also suggest that within this population, large body
size of males provides more than just a competitive mating
advantage. That cohorts with larger mean body sizes
produced more surviving offspring supports a previously
hypothesised link between male body size and overall quality
and/or quantity of offspring.
DISCUSSION
Understanding how phenotypic variation interacts with selec-
tive mortality and density dependence can greatly improve
our understanding of recruitment. It is clear that selective
mortality can be substantial, with episodes of selection fre-
quently removing more than half of the individuals from a
cohort. Moreover, variation in selective mortality among
cohorts can also be large, suggesting considerable effects on
recruitment variability. Here, we have described a framework
to evaluate how phenotypic variation can result in systematic
differences in selective mortality. This framework can be
extremely valuable for making sense of the apparent variabil-
ity in selection and for understanding variation in population
replenishment.
Our examples illustrate that the relationships between phe-
notypes and early life survival may be relatively constant. In
contrast, the distributions of phenotypes that affect survival
appear to differ substantially among cohorts. It is the latter
phenomenon that may be responsible for much of the varia-
tion in selective mortality. A major implication is that if t-
ness surfaces can be estimated, and one has information on
the distribution of phenotypes that affect survival, then
recruitment may be reasonably predictable. In fact, informa-
tion on phenotypic variability and selective mortality can be
used in a manner similar to stockrecruitment models: mea-
sured attributes of the system (e.g. phenotype distributions
and tness surfaces) can be used to predict average values of
recruitment.
Although tness surfaces can change with environmental
conditions, situations in which tness surfaces are essentially
constant may not be particularly rare. However, if tness sur-
faces are commonly non-linear, they may be difcult to
describe. The challenge for biologists will be to conduct stud-
ies with enough replicate measures of selection to reconstruct
tness surfaces and rigorously evaluate whether tness sur-
faces may be treated as constant. Although we acknowledge
that for shes, such studies are rare, evidence of constancy in
tness surfaces has regularly been observed for other taxa.
For example, systematic and strong relationships between
phenotype distributions and selection measurements have been
Figure 7 Combined effects of mean body size and number of adult males
on recruitment of steelhead trout. Recruitment is dened as the number
of offspring (both sexes) that returned to spawn as adults. Response
surface illustrates the maximum likelihood t of a combined phenotype-
and density-dependent model (eqn 6 in the main text). To display the
surface, within-cohort variance was held at the overall average. Actual
predictions of recruitment are based on variation in both means and
variances. Original data from Seamons et al. (2007).
2014 John Wiley & Sons Ltd/CNRS
752 D. W. Johnson et al. Review and Synthesis
observed in well-replicated studies of selection in populations
of insects (e.g. Weis et al. 1992), birds (e.g. Reed et al. 2006;
Brommer & Rattiste 2008; Charmantier et al. 2008), and
mammals (e.g. Wilson et al. 2006). These observations suggest
that the general methods described in this study may be
widely applicable, even if constant tness surfaces are not the
norm. Moreover, when it is clear that tness surfaces do vary
with other features of the local environment (e.g. density or
any other measurable characteristic), such effects may be
incorporated into the function describing the rate of selective
mortality (e.g. f
z
can become f
z,N
in the case of density-depen-
dent selection; Appendix S2).
When mortality is density dependent, information on phe-
notype distributions and selective mortality can add another
dimension to traditional stockrecruitment models. Simple,
density-dependent models usually do a reasonable job of
describing non-linear relationships between density and
recruitment. However, such models typically do a poor job of
explaining variability in real data (Iles 1994; Myers 2001). In
other words, density-dependent models capture the central
tendency of recruitment, but they cannot explain why certain
cohorts deviate from this central tendency. Several studies
have implied that accounting for some forms of phenotypic
variation (particularly changes in the age/size composition of
the spawning population) in stockrecruitment models can
improve their performance (Marteinsdottir & Thorarinsson
1998; Scott et al. 1999; Lucero 2009; Brunel 2010). However,
both density dependence and the relationship between pheno-
type(s) and survival are often strongly non-linear. Because of
this, simple approaches to analysing the effects of phenotype
and density on recruitment (e.g. multiple regression) are unli-
kely to be adequate. For example, on curvilinear tness sur-
faces, differences in the variances of cohorts can lead to large
differences in recruitment (eqn 6). For shes, within-cohort
variance is highly variable among cohorts (from our review,
median CV = 23%, range = 2.664%), and likely to be a per-
sistent source of recruitment variation. By starting with indi-
vidual survival probabilities, and accounting for the
distributions of individuals within cohorts, we can generate
models of density-dependent recruitment that properly
account for the non-linear effects of phenotype on survival.
CONCLUSIONS
Our review and synthesis of selection measurements suggests
that for recruiting cohorts of shes, most mortality is selective
mortality. The amount of selective mortality is also highly
variable among cohorts, suggesting that if we have a better
understanding of why selective mortality varies, then we can
improve our understanding of recruitment. Through several
empirical examples where selection has been well studied, our
analyses show that tness surfaces may be relatively constant,
but strongly non-linear. These results suggest that much of
the variation in mortality during the recruitment process may
be predictable and a direct consequence of variation in the
distribution of phenotypes that are important for survival.
The true utility of a framework that describes the combined
effects of phenotypic variation, selective mortality and density
dependence (where applicable) on recruitment is that it will
allow one to evaluate both the short- and long-term conse-
quences of variation in phenotypes. For shes, among-cohort
variation in the distribution of early life traits can be inu-
enced by several factors including temperature (Macpherson
& Raventos 2005; Sponaugle et al. 2006), parental effects
(Heath et al. 1999; McCormick 2006; Johnson et al. 2011),
location of larval development (Hamilton et al. 2008; Shima
& Swearer 2009) and/or source population (e.g. Post & Prank-
evicius 1987). In the short term, knowing the shape of the t-
ness surface will yield insight into how variation in these
environmental factors ultimately translates into variation in
recruitment. In the long term, an accurate description of the
tness surface will be useful in that it will allow investigators
to predict the effects of long-term changes in characteristics of
larvae and juveniles. For example, it is expected that early life
traits will change in response to factors such as shery selec-
tion (Munch et al. 2005; Walsh et al. 2006; Johnson et al.
2011) and climate change (e.g. Munday et al. 2009; Franke &
Clemmesen 2011; Baumann et al. 2012). By understanding
how such changes in phenotypes will ultimately affect recruit-
ment, we will be able to anticipate how changes in the abiotic
and biotic environment will affect both the quality of individ-
uals in the population, and the populations capacity for resis-
tance and/or resilience to environmental change.
ACKNOWLEDGEMENTS
We thank Robert Warner, Todd Seamons, Liz Pasztor and two
anonymous referees for their helpful comments on an earlier
draft of the manuscript. This work was conducted while D.W.J.
was supported by a postdoctoral fellowship from Scripps Insti-
tution of Oceanography. During the preparation of this manu-
script, both S.S. and B.X.S. were supported in part by grants
from the National Oceanic and Atmospheric Administration
(NA11NOS4780045 to S.S., NA10OAR4320156 to B.X.S.).
AUTHORSHIP
D.J., K.G.C., S.S. and B.X.S. conceived the study. D.J. wrote
the rst draft of the manuscript, and all authors contributed
substantially to the revisions.
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SUPPORTING INFORMATION
Additional Supporting Information may be downloaded via
the online version of this article at Wiley Online Library
(www.ecologyletters.com).
Editor, Mikko Heino
Manuscript received 26 December 2013
First decision made 31 January 2014
Second decision made 18 February 2014
Manuscript accepted 24 February 2014
2014 John Wiley & Sons Ltd/CNRS
Review and Synthesis Selective mortality and recruitment 755