The origins and drivers of sexual size dimorphism in sharks

Abstract

While sexual size dimorphism (SSD) is abundant in nature, there is huge variation in both the intensity and direction of SSD. SSD results from a combination of sexual selection for large male size, fecundity selection for large female size and ecological selection for either. In most vertebrates, it is variation in the intensity of male–male competition that primarily underlies variation in SSD. In this study, we test four hypotheses regarding the adaptive value of SSD in sharks—considering the potential for each of fecundity, sexual, ecological selection and reproductive mode as the primary driver of variation in SSD between species. We also estimate past macroevolutionary shifts in SSD direction/intensity through shark phylogeny. We were unable to find evidence of significant SSD in early sharks and hypothesise that SSD is a derived state in this clade, that has evolved independently of SSD observed in other vertebrates. Moreover, there is no significant relationship between SSD and fecundity, testes mass or oceanic depth in sharks. However, there is evidence to support previous speculation that reproductive mode is an important determinant of interspecific variation in SSD in sharks. This is significant as in most vertebrates sexual selection is thought to be the primary driver of SSD trends, with evidence for the role of fecundity selection in other clades being inconsistent at best. While the phylogenetic distribution of SSD among sharks is superficially similar to that observed in other vertebrate clades, the relative importance of selective pressures underlying its evolution appears to differ.

Full text

Ecology and Evolution. 2024;14:e11163.  
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https://doi.org/10.1002/ece3.11163
www.ecolevol.org
1 | INTRODUCTIO N
Differences in body size between organisms have an array of
physiological, biomechanical, ecological and evolutionary im-
plications (Blanckenhorn, 2000; Brown et al., 1993; Woodward
et al., 2005). Such differences are of course present between taxa
but also between the sexes—a phenomenon referred to as sexual
size dimorphism or SSD (Horne et al., 2020). SSD is abundant in the
natural world and has been studied in a range of taxa (Monnet &
Cherry, 2002; Parker, 1992; Shine, 19 94). The magnitude and direc-
tion of SSD are known to be highly variable, as in some species fe-
males reach larger sizes (female- biased SSD), whereas in others, it
Received:29Februar y2024
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Accepted :5March2024
DOI : 10.10 02/ec e3.11163
RESEARCH ARTICLE
The origins and drivers of sexual size dimorphism in sharks
Joel H. Gayford1,2 | Phillip C. Sternes2,3
This is an op en access ar ticle under the terms of the CreativeCommonsAttribution License, which permits use, distribution and reproduction in any medium,
provide d the original work is properly cited.
©2024TheAut hors.Ecology and Evolution published by John Wiley & Sons Ltd.
1Depar tment of Life S ciences, Silwood
Park Campus, Imperial College London,
London, UK
2Shark Measurements, London, UK
3Depar tment of Evolut ion, Ecolog y
and Organismal Biology, University of
Califo rnia,Riverside,California,USA
Correspondence
Joel H. Gayford, De partment of Life
Science s, Silwood Park Campus, Imperial
College L ondon, 6 New Road Lewes,
London B N7 1YW, UK.
Email: jhg19@ic.ac.uk
Abstract
While sexual size dimorphism (SSD) is abundant in nature, there is huge variation in
both the intensity and direction of SSD. SSD results from a combination of sexual
selection for large male size, fecundity selection for large female size and ecological
selection for either. In most vertebrates, it is variation in the intensity of male–male
competition that primarily underlies variation in SSD. In this study, we test four hy-
potheses regarding the adaptive value of SSD in sharks—considering the potential for
each of fecundity, sexual, ecological selection and reproductive mode as the primary
driver of variation in SSD between species. We also estimate past macroevolutionary
shifts in SSD direction/intensity through shark phylogeny. We were unable to find
evidence of significant SSD in early sharks and hypothesise that SSD is a derived state
in this clade, that has evolved independently of SSD observed in other vertebrates.
Moreover, there is no significant relationship between SSD and fecundity, testes mass
or oceanic depth in sharks. However, there is evidence to support previous specula-
tion that reproductive mode is an important determinant of interspecific variation in
SSD in sharks. This is significant as in most vertebrates sexual selection is thought to
be the primary driver of SSD trends, with evidence for the role of fecundity selection
in other clades being inconsistent at best. While the phylogenetic distribution of SSD
among sharks is superficially similar to that observed in other vertebrate clades, the
relative importance of selective pressures underlying its evolution appears to differ.
KEY WORDS
Chondrichthyes, ecology, Elasmobranchii, natural selection, sexual conflict, sexual selection
TAXONOMY CLASSIFICATION
Zoology

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is males that are typically larger (Isaac, 2005; Rohner et al., 2018;
Webb & Freckleton, 2007). Empirical studies and life- history the-
ory predict that variability in SSD (both in terms of direction and
magnitude) is likely to be driven by the relative strengths of sexual
selection, fecundity selection and ecological selection (Fairbairn
et al., 20 07). Strong f ecundity sele ction is thought t o result in female-
biased SSD, whereas strong sexual selection (specifically male–male
competition) is thought to favour the evolution of male- biased SSD
(Fairbairn et al., 2007; Head, 1995; Janicke & Fromonteil, 2021;
Pa rke r, 1992) and ecological selec tion can favour either male- biased
or female- biased SSD (Main et al., 1996; Shine, 1989; Wearmouth &
Sims, 2008). In all cases, these are general trends, and examples
are known of sexual selection favouring smaller males or variation
in reproductive tac tics as opposed to male- biased SSD (Pilastro
et al., 1997). In reality, it is likely that many selective pressures con-
tribute to the evolution of SSD, but current studies are primarily re-
stricted to inferences on the basis of correlation between SSD and
various facets of life history and ecology. The degree to which each
of these processes appears to influence SSD in different clades dif-
fers greatly, and only through rigorous empirical studies of SSD and
its correlates can we hope to understand its adaptive value (Horne
et al., 2020). In light of the controversy regarding selective driv-
ers of SSD in vertebrates and historic bias towards cert ain clades
(Pincheira- Donoso & Hunt, 2017 ) there is a need for additional
studies of SSD targeting diverse radiations throughout vertebrate
phylogeny.
Sharks (Elasmobranchii: Selachii) are a morphologically and
ecologically disparate group of vertebrates distributed globally in
marine and freshwater ecosystems (Heithaus et al., 2010; Heupel
et al., 2014; Sternes & Shimada, 2020). Sharks exhibit a vast de-
gree of variation in life- history parameters and reproductive
biology, making them ideal candidate taxa for the study of SSD
and its evolutionary drivers (Carrier et al., 2004; Cortés, 2000).
Moreover, as the sister taxon to Osteichthyes, macroevolu-
tionary trends within Chondrichthyes are of great relevance
to our understanding of character transitions and trait evolu-
tion in jawed vertebrates (Hara et al., 2018; Stein et al., 2018;
Venkatesh et al., 2014). Sexual dimorphism is abundant in sharks
(Gayford, 2023), and indeed, SSD has been reported in many spe-
cies (Colonello et al., 2020; Sims, 2005). Existing studies have
speculated that the magnitude and direction of SSD in sharks may
relate to differences in reproductive mode and/or the intensity
of sexual selection (Colonello et al., 2020; Sims, 2005). The first
of these hypotheses suggests that selection on large female body
size may be relaxed in oviparous t axa relative to matrotrophic taxa
due to the ex ternal development of embr yos and extensive re-
productive period (Sims, 2005). It has also been suggested that
sexual selection is more intense in oviparous elasmobranchs, and
that this would favour the evolution of male- biased SSD (Colonello
et al., 20 07, 2020). Indeed, in most vertebrate groups, it has been
found that variation in SSD between species is primarily driven
by variation in the intensit y of male–male competition (Fairbairn
et al., 20 07; Head, 1995; Horne et al., 2020; Parker, 1992). While
sexual conflict and sexual selection are thought to be abundant in
elasmobranchs (Gayford, 2023; Rowley et al., 20 19), a lack of data
have impeded our understanding of macroevolutionary changes
in these traits, and the extent to which they might correlate with
SSD. Impor tantly, given the abundance of sexual segregation in
elasmobranchs (Mucientes et al., 2009), and the high variation in
fecundity between species (Cortés, 2000, 2008), it is likely that all
three of these factors contribute to the evolution of SSD, and one
study considering ‘fishes’ (including several elasmobranch species)
found that the observed distribution of SSD was consistent with
selection for increased male size rather than fecundity selec tion
(Horne et al., 2020), however, the predominance of bony fish in
this data set means that there is little reason to suggest these re-
sults should be indicative of the evolutionary drivers of SSD oper-
ating through shark phylogeny.
In this study, we use comparative phylogenetic methods and a
large, diverse data set to investigate the evolution of SSD in sharks—
an ancient group displaying a broad array of life- histories and repro-
ductive modes. Primarily, we fit different evolutionary models to test
the following four hypotheses: that post- copulatory sexual selec-
tion varies systematically with the strength and/or direction of SSD
(1), that fecundity selection varies systematically with the strength
and/or direction of SSD (2), that ecology varies systematic ally with
the strength and/or direc tion of SSD (3) and that reproductive mode
varies systematically with the strength and/or direction of SSD (4).
We also perform evolutionary model tests and ancestral state recon-
struc tion to provide insight into the evolutionary dynamics underl ying
macroevol utionary shif ts in SSD. Importantly, while we do not directly
measure selection in any form, to test hypotheses relating to sexual
and fecundity selec tion, we use life- history traits generally thought to
covary strongly with these selective regimes. This is the first rigorous
quantitative study to address the evolution of SSD in sharks, directly
addressing speculative hypotheses that have arisen in the literature.
Our analyses uncover systematic patterns in the distribution of SSD
defined by differences in reproductive mode but fail to recover any
evidence of differences in SSD delineated by sexual selection, repro-
ductive output or depth. Given the phylogenetic placement of sharks
and the degree of life- history variation they exhibit, these results are
of paramount importance to our understanding of the adaptive value
of SSD and sexual dimorphism more broadly.
2 | METHODOLOGY
2.1 | Data collection
The following biological data were extracted from the reference
book ‘Sharks of the World: a Complete Guide’ (Ebert et al., 2021):
maximum length (cm), leng th at birth (cm), length at maturity for
each sex (cm), reproductive mode (matrotrophic or oviparous), mini-
mum litte r size, maximum litter size, habitat t ype (benthic, benthope-
lagic, pelagic) and depth (shallow, intermediate, deep). For oviparous
taxa, eggcase leng th was also recorded. Quantitative measures of
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minimum, median and maximum depth were also gathered from
FishBase (Froese & Pauly, 2023). For all measurements if upper
bounds were unknown, the lower bound was taken as the default
value. Where unverified size records existed, they were ignored, and
where a range of values were provided for a given measurement the
median value was taken. Species for which the length of maturity for
both sexes and/or maximum leng th were not known were excluded,
as were species whose phylogenetic placement remains unresolved.
The relative strength of sexual selection was modelled as body size-
corrected testes mass (a common proxy for post- copulatory sperm
competition) and data were extracted from Rowley et al. (2019).
Two measures of SSD were defined using the body size data
extracted from ‘Sharks of the World: a Complete Guide’ (Ebert
et al., 2021): male- to- female ratio (MFR) is the ratio of median length
at sexual maturity bet ween males and females, and sexual dimor-
phism percentage (SD%) is the percentage of maximum total length
corresponding to the dif ference in median length at sexual matu-
rity between the two sexes. SD% measures the magnitude of SSD,
whereas MFR measures the direction of SSD. Thus, the absence of
SSD would result in an MFR value of one and an SD% value of zero.
To take into account size variation between taxa, length at bir th and
eggcase length were standardised, dividing them by maximum total
length. Minimum, median and maximum litter sizes were multiplied
by this standardised value of neonate/eggcase length (depending on
whether the taxon in question was matrotrophic or oviparous) to
provide a more reasonable estimate of reproductive output. These
measures will henceforth be referred to as minimum, median and
maximum reproductive output.
Phylogenetic data were ex tracted from Stein et al. (2018), and
the resulting time- scaled phylogeny was pruned to match the data
using the function match.phylo.data in the R package picante (Kembel
et al., 2010). The final data set includes 339 taxa representing a
range of ecologies and including members of all major selachimorph
radiations (Figure 1).
2.2 | Data analysis
AllanalyseswerecarriedoutintheR statistical environment (R Core
Tea m, 2023). Prior to analyses, the variables raw minimum litter size,
raw median litter size, raw maximum litter size, minimum reproduc-
tive output, median reproductive output and maximum reproductive
output were log- transformed. Minimum depth (m), median depth (m)
and maximum depth (m) were also log- transformed, however, due to
the presence of zero values, a constant value of 1 was added to all val-
ues prior to log- transformation. Testes mass was not log- transformed
due to low skew and the presence of negative values. Reproduc tive
mode was coded as a binary variable with matrotrophy represented
by a value of 1, and oviparity represented by a value of 0.
To compare different adaptive hypotheses for the evolution of
SSD, we fit a series of phylogenetic linear models to our data using
the package phylolm (Ho et al., 2016), testing for possible evolu-
tionary relationships between SSD (SD% and MFR) and potential
biological/ecological correlates. For each of SD% and MFR, 8 mod-
els were fit initially, each including one of the following covariates:
reproductive mode, testes mass, minimum reproductive output,
median reproductive output, maximum reproductive output, min-
imum depth (m), median depth (m), and maximum depth (m). An
Ornstein–Uhlenbeck (OU) covariance model was used to provide the
phylogenetic correction for these models. OU- based models of trait
variation are typically a prerequisite for testing adaptive hypothe-
ses, as unlike Brownian motion models they allow traits to evolve
towards one or more optima (Cressler et al., 2015). In all cases, 100
independent bootstrap replicates were generated.
Due to discr epancies in the num ber of taxa for which potential bi-
ological/ecological correlates are known, we subsequently repeated
these analysesusinga reducedsamplesize,permitting directAIC-
based comparison of the resulting models. We also fit more complex
phylogenetic linear models including all possible combinations of the
following covariates: reproductive mode, depth (the depth variable
with the m ost explanator y AIC value was se lected), repro ductive
output (the reproductive output variable with the most explanatory
AICvaluewasselected).Toprovideacomparativebaselinebywhich
to assess these models, we also fit null models without any covari-
ates. We chose this approach instead of fitting models with all pos-
sible combinations to reduce model redundancy. Testes mass was
excluded from these combined models as the small number of taxa
for which this parameter is known would substantially reduce the
statistical power of these analyses, which require equivalent sample
samplesizeforAIC-basedmodelselection.
To test the validity of assumptions made by OU- based mod-
els, we used the package mvMORPH (Clavel et al., 2015) to fit sin-
gle (BM1 and OU1) and multi- peak (BMM and OUM) BM and OU
models to both SSD parameters (SD% and MFR), selecting the
best-supportedmodeloftraitevolutiononthebasisofAICcvalues
(Posada & Buckley, 2004). Finally, to map the evolutionary histor y of
SD% and MFR , ancestral state reconstruction was performed upon
both traits in the package phytoo ls (Revell et al., 2008).
All data used in this study can be found in the Supporting
Information associated with the article.
3 | RESULTS
Our evolutionary model test revealed that in the cases of both SD%
and MFR, Ornstein–Uhlenbeck (OU) models of trait evolution bet-
ter explain the phylogenetic distribution of SSD than Brownian mo-
tion (BM) models (Table 1). Multi- peak OU models received the most
support, whereas single- peak BM models received the least support
(Table 1).
Univariate phylogenetic linear models using the full data set
recovered one statistically significant relationship between SSD
potential covariates (Table 3). Reproductive output correlated sig-
nificantly with both SD% and MFR (Table 3).Allotherrelationships
werenon-significantandcouldnotbecomparedonthebasisofAIC
due to differential sample sizes.
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Univariate phylogenetic linear models using a reduced data set
failed to recover any statistically significant relationships between
SSD and other potential covariates (Table 3). In the case of both SD%
and MFR, null models excluding all covariates received greater sup-
port than any covariate models (Table 2).
Multivariate phylogenetic linear models did not receive greater
support than the null model in either the case of SD% or MFR
(Tables 3 and 4). In both cases, multivariate models containing
reproductive mode and reproductive output only received more
support than those incorporating depth (Table 4). While none of
FIGURE 1 Time-scaledmolecularphylogenydisplayingthetaxaandinterrelationshipsutilisedinthisstudy.Branchlengthswere
obtained from Stein et al. (2018). Silhouettes are representative taxa from various selachimorph radiations included in the study. Silhouette
images obtained online have been dedicated to the public domain.
SSD measure Covariance model Log- likelihood AICc ΔAICc
SD% BM1 −621.3745 1247 –
SD% BMM −575.2937 1159 −88
SD% OU1 −458 .3395 925 −32 2
SD% OUM −323.1288 659 −588
MFR BM1 114.1443 −2 24 –
MFR BMM 11 7.0 4 4 2 −22 6 −2
MFR OU1 240..8408 −474 −25 0
MFR OUM 351 .159 8 −690 −466
Note: See methodology for details of the covariance models.
Abbreviations:AIC ,Akaikeinformationcriteria;MFR,male-to-femaleratio;SSD,sexualsize
dimorphism.
TABLE 1 Outputfromtheevolutionary
model test, including difference
covariance models fit to SSD data
andvaluesformodelsupport(AICc,
log- likelihood).
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these models were favoured over the null model, a significant
relationship between median reproductive output and MFR was
found in the model incorporating reproductive output and repro-
ductive mode (Table 4).
Ancestral state reconstruction of both SSD measures esti-
mated an ancestral selachian with an SD% value of 10.80 (95% CI:
0≤x≥34.05
) and an MFR value of 0.868 (95% CI:
0.59 ≤x≥1.15
),
with multiple independent increases and decreases in sexual di-
morphism occurring since (Figure 2). There is thus no evidence to
suggest that the male and female ancestral selachimorphs differed
significantly in size.
4 | DISCUSSION
In this study, we aimed to improve our understanding of the evolu-
tion of SSD in vertebrates by testing for relationships between the
direction and magnitude of SSD and (1) the intensity of sexual se-
lection, (2) the intensity of fecundit y selection, (3) ecology and (4)
reproductive mode in sharks. We also estimated past macroevolu-
tionary shifts in SSD magnitude/direction across shark phylogeny.
Contrary to other ver tebrate clades, we fail to recover any evidence
for relationships between SSD and fecundity, sexual selection or
ecology (Tables 2–4). However, we do find evidence to support pre-
vious speculation that there exists some relationship between SSD
and reproductive mode (Colonello et al., 2020). Regarding the evolu-
tionary origins of SSD in sharks, we rather surprisingly fail to recover
evidence of significant SSD in early selachians. In the following sec-
tions, we expand on these results, what they might tell us about the
evolution of SSD in vertebrates, and what future advances will be
necessary to better understand trends in SSD among car tilaginous
fishes.
4.1 | SSD and reproductive mode: Morphological
constraint or sexual selection?
Our results support a previous, speculative hypothesis that re-
productive mode is an important determinant of interspecific
variation in SSD among shark species (Table 2). Indeed, our results
suggest that oviparous t axa are associated with relatively low SD%
values and relatively large MFR values, whereas matrotrophic taxa
(including placental and aplacental viviparity) have relatively large
SD% values and relatively low MFR values (Table 2). This suggests
that male- biased SSD is more prevalent in oviparous shark species,
whereas viviparous taxa are more likely to exhibit female- biased
SSD. It is also worth noting that SSD is generally less intense in
oviparous species compared to viviparous species, as evidenced
by differential SD% values (Table 2). While these significant results
were not recovered in subsequent analyses ( Tables 3 and 4), this is
not surprising as only one oviparous taxon was included in the re-
duced data set. The role of reproductive mode in determining the
direction of SSD in sharks has been mentioned in previous studies
(Colonello et al., 2020; Sims, 2005), however, until now this has
been a purely speculative hypothesis, with no phylogenetically-
informed evidence.
Male- biased SSD was previously suggested to be more preva-
lent in oviparous taxa for two reasons: relaxed selection on large
female body size due to extended reproductive period and external
development of embryos (Sims, 2005) and elevated levels of sexual
selection for increased male body size relative to matrotrophic spe-
cies (Colonello et al., 20 07, 2020). The first of these factors appears
superficially similar to fecundit y selection but differs in that it is
the spatio- temporal distribution of reproductive output rather than
the magnitude of reproductive effort that differs between species.
Selection for increased female size in matrotrophic shark species
is logical given the number and size of pups produced and the ex-
tendedgestationperiodofmanysharks(Auetal.,2008; Tokunaga
et al., 2022). Differences in the nature of sexual selection between
oviparous and matrotrophic shark species are more problematic: in
this study, we focused on testes mass—commonly used as a proxy
for the intensity of post- copulatory sexual selection, and failed to
find any relationship bet ween this variable and SSD ( Tables 2–4).
Moreover, sexual selection is only thought to favour the evolution
of male- biased SSD, where a high degree of territoriality, sperm
competition or parental care is observed (Horne et al., 2020). Direct
parental care is unknown in elasmobranchs (Carrier et al., 2004),
and indeed would be unexpected given the prevalence of multiple
paternit yin theclade(Armada-Tapiaet al.,2023). There is no evi-
dence of widespread territoriality in elasmobranchs and although
sperm competition is known, this data come from a tiny fraction
of extant species (Rowley et al., 2019). Therefore, we suggest that
this relationship between reproductive mode and SSD results from
relaxed selection of female body size in oviparous taxa (due to
spatio- temporal differences in the distribution of reproductive ef-
fort) rather than sexual selection. Importantly, this only provides an
explanation for the presence or absence of female- biased SSD and
does not explain cases of male- biased SSD.
4.2 | SSD, fecundity and ecology
Despite their importance as a determinant of SSD in other ver-
tebrates, we found no evidence for correlation between the
streng th/direction of SSD and either fecundity or ecological se-
lection in sharks (Tables 2–4). Increased female body size is gener-
ally thought to convey greater fecundity and reproductive energy
output, and thus in species where fecundity selection is stronger,
SSD is expected to be greater in magnitude and female- biased
(Head, 1995; Horne et al., 2020; Reeve & Fairbairn, 1999). It is im-
portant to note that across vertebrate diversity this hypothesised
relationship between fecundity selection and SSD has received
inconsistent support, and other factors such as ecological selec-
tion are now known to underlie many cases of female- biased SSD
(Pincheira- Donoso & Hunt, 2017). Our results provide some nu-
ance to ideas of fecundity and reproduc tive biology influencing
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TABLE 2 Outputfromphylogeneticlinearmodelsusingthefulldataset,includingtheevolutionaryparametersα and
𝜎2
.
SSD measure Covariate Scaling coefficient p value Log- likelihood AICc α
𝝈2
SD% Testes mass 0.322321 .9630803 −58.47 126 .95 7.41e−0 3 6.94e−01
SD% Minimum depth 0.0509014 .0773 −381.3 772.6 3.47e −03 1.78e−03
SD% Median depth 0.045666 .4182 −380.3 770.6 3.94e−03 1.75e− 03
SD% Maximum depth 0.0084177 .8738 − 40 9.6 8 29.1 4.22e−0 3 2.05e−03
SD% Minimum reproductive output 0.113 094 .1482 −240.7 491.3 2.63e−03 2 .10e−03
SD% Median reproductive output 0.074045 .4954 −2 38 .1 486.2 2 .67e−03 1.80e−03
SD% Maximum reproductive output −0.0026656 .9776 −247. 3 504.5 3 .37e−0 3 2.56e−03
SD% Reproductive mode 3.60979 .03465 −108 1 2171 3.45e−03 0.2 011159
MFR Testes mass −0.039473 .6305 21.47 −32.93 6.56e−03 8.86e−05
MFR Minimum depth −0.0029959 .4124 2 27. 7 −445.4 1.68e−03 3.15e−05
MFR Median depth −0.0092905 .1993 228.4 −446.8 1.96 e−03 3 .02e−05
MFR Maximum depth −0.0040548 . 5510 241.6 −473.3 2.43e−03 4.04e−05
MFR Minimum reproductive output −0.0117264 .21492 160.0 −309.9 1.46e−03 2.40e−05
MFR Median reproductive output −0.021151 .1099 158.6 − 307. 3 1.60e−03 2.36e−05
MFR Maximum reproductive output −0.013800 .22238 164 3 −318.6 1.68e−03 2.53e−05
MFR Reproductive mode −0.053258 .01923 296.7 −5 83.3 3.32e−03 4.078e−05
Note:AICvaluescannotbecomparedduetonon-equivalentsamplesizesbetweenmodels.
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TABLE 3 Outputfromphylogeneticlinearmodelsusingthereduceddataset,includingtheevolutionar yparametersα and
𝜎2
.
SSD measure Covariate Scaling coefficient p value Log- likelihood AICc α
𝝈2
SD% None (null) NA NA −205.9 419.7 2.04e−03 1.46e−03
SD% Minimum depth 0.0 40111 .294 −205.3 420.6 2.25e−03 1.39e−03
SD% Median depth 0.031405 .6567969 −205.8 421.6 2.20e−03 1.38e−03
SD% Maximum depth 0.018139 .793286 −205.8 421.7 2.13e−03 1 .41e− 03
SD% Minimum reproductive output 0.078698 .3395 −205.4 420.8 2.23e−03 1.54e− 03
SD% Median reproductive output 0.069694 .5373 −205.7 421.3 2.19e−03 1.50e−03
SD% Maximum reproductive output 0.003578 .9717 −205.9 421.7 2.05e−03 1.46e−03
SD% Reproductive mode 0.858564 . 2157 −205.1 420.2 2.23e−03 1.41e− 03
MFR None (null) NA NA 134. 8 −261.5 2.27e −03 2.05e−05
MFR Minimum depth 0.00021796 .96328 134. 8 −259. 5 1.22e−03 2.05e−05
MFR Median depth −0.0090363 .2958 135.2 −260 .5 1.46e−03 1.84e−05
MFR Maximum depth −0.0079795 .345 135.2 −260.3 1.42e− 03 1.86e−05
MFR Minimum reproductive output −0.008537 .39570 135.1 −26 0. 2 1. 27e− 03 2.04e−05
MFR Median reproductive output −0.023748 .08475 136 .3 −262. 5 1.37e−03 2. 07e− 05
MFR Maximum reproductive output −0.017577 .1520 135.8 −261 .6 1.32e−03 1.99e−05
MFR Reproductive mode −0.085913 .3170 135.3 −2 60 .5 1. 29e−03 1.98e−05
Note:AICvaluescanbecompareddirectlyduetoequivalentsamplesizesunderlyingallmodels.
Abbreviations:AIC ,Akaikeinformationcriteria;MFR,male-to-femaleratio;SSD,sexualsizedimorphism.
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SSD, as in a clade with unparalleled variation in reproductive bi-
ology, it is spatio- temporal variation in reproductive output as
opposed to reproductive output itself that appears to influence
female body size (Table 2). Fecundity data are lacking for the ma-
jority of oviparous species however, and additional studies will be
required to verify the extent to which fecundity selection may the
strength of correlation between different measures of reproduc-
tive output and fecundity selection.
Neglected in several evolutionary studies of SSD in fishes (Horne
et al., 2020; Parker, 1992), we tested for relationships between an
important facet of ecology and both the strength and direction of
SSD in sharks but failed to find any significant correlation (Tables 2–
4). It is generally accepted that ecological selection acts on body
size in vertebrates (Blanckenhorn, 2000; Sheridan & Bickford, 2011;
Shine, 1989), and that in some systems, SSD reflects a balance or
trade- off between natural selection and sexual selec tion (Nudds &
Kaminski, 1984; Pearson et al., 2002; Shine, 19 89; Wikelski &
Trillmich, 1997 ). We used depth as a measure of ecology as the
shallow- deep continuum is known to have been an influential force
shaping morphological evolution in elasmobranchs (López- Romero
et al., 2023; Sorenson et al., 20 14), and it is generally recognised that
the complexity and diversity of shallow- water marine environments
(Martinez et al., 2021; Miller et al., 2022) leads to a gradient of rel-
atively weak to strong ecological selection with increasing depth.
In shallow- water environments, greater ecological complexity and
higher competition levels could favour enhanced niche/resource
partitioning (Cloyed & Eason, 2017), in turn favouring the evolution
of stronger SSD, which could be either female or male- biased de-
pending on the system in question. Resource partitioning has been
reported in a number of shark species (Curnick et al., 2 019; Kinney
et al., 2011) and is known to contribute to SSD in other taxa (Nudds &
Kaminski, 1984), but our results suggest that depth is not an im-
portant driver of SSD in sharks (Tables 2–4). It is also worth men-
tioning that depth is an important determinant of light penetration,
which in some fishes shapes female preference and consequently
pre- copulatory sexual selection (Gray et al., 2008; Heinen- Kay
et al., 2015). The role of female preference in sexual selection in
sharks is unknown but it is important to recognise that ecological
variables such as depth correlate not only with ecologic al selection
but with other potential selective pressures including some facets
of sexual selection and reproductive mode (Katona et al., 2023).
Additionalstudiesincorporatingotherfacetsofecologyareneeded,
but on the basis of our results, there is no evidence for significant
relationships between ecological selection and SSD in sharks.
4.3 | Macroevolutionary shifts in SSD among
sharks and other vertebrates
While the distribution of SSD through shark phylogeny (Figure 2)
does not di ffer fundamen tally from that ob served in other ve rtebrate
clades , our results have imp ortant impli cations for our und erstanding
of the adaptive value of SSD. The drivers of SSD evolution have been
TABLE 4 Outputfrommultivariatephylogeneticlinearmodelsusingthereduceddataset,includingtheevolutionar yparametersα and
𝜎2
.
SSD measure Covariates Scaling coefficients p values Log- likelihood AIC α
𝝈2
SD% Minimum depth, reproductive mode 0.044437, 0.916676 .2422, .1816 −204.4 420.9 2. 52e−03 1.33e−03
SD% Minimum depth, minimum reproductive
output
0.036634, 0.070119 .3414, . 3969 −205.0 421.9 2.43e−03 1 .47e−03
SD% Minimum depth, minimum reproductive
output, reproductive mode
0.040833, 0.093483, 1.064259 .2837, .2645, .1274 −203 .8 421. 6 2.85e−03 1 .41e− 03
SD% Minimum reproductive output,
reproductive mode
0.10124 6, 1. 02224 4 . 22 57, .14 76 −204.4 420.7 2.54e−03 1.50e−03
MFR Minimum depth, reproductive mode −0.010104,−0.093573 .2413, .2663 135.9 −2 59.7 1.60e−03 1.74e− 05
MFR Minimum depth, median reproductive
output
−0.0067935,−0.0220288 .43 57, .11 29 136.5 −2 61.1 1.5 7e−03 1.90 e−05
MFR Minimum depth, median reproductive
output, reproductive mode
−0.0079247,−0.0268892,−0.1318313 .35852, .05779, .12472 137.7 −261. 4 1.81e− 03 1.75e−05
MFR Median reproductive output,
reproductive mode
−0.028617,−0.128467 .04253, .14125 137. 3 −262 .7 1. 52e−0 3 1.95e−05
Note:AICvaluescanbecompareddirectlyduetoequivalentsamplesizesunderlyingallmodels.
Abbreviations:AIC ,Akaikeinformationcriteria;MFR,male-to-femaleratio;SSD,sexualsizedimorphism.
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FIGURE 2 Ancestralstatereconstructionsforsexualdimorphismasmale–femaleratio(a)andapercentageofmaximumtotallength
(b) superimposed upon the selachimorph phylogeny, displaying the evolutionary histories of these t wo traits.
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studied in a number of vertebrate groups (including mammals, birds,
reptiles, amphibians and fishes) and in most cases, it is sexual selec-
tion for increased male size that appears to be the most important
factor, with evidence for fecundity selection driven SSD evolution
inconsistent or absent despite the dominance of female- biased SSD
(Horne et al., 2020; Monroe et al., 2015; Seehausen et al., 2008). In
the absence of vertebrate- wide comparative phylogenetic studies,
this would suggest that broadly across vertebrate diversity sexual
selection on male body size is stronger than fecundit y selection on
female body size. In sharks, it appears that neither of these factors
plays an important role in shaping SSD trends (Tables 2–4), suggest-
ing that the adaptive landscape underlying SSD has undergone a
major shif t at some point during gnathostome phylogeny.
Intriguingly, our ancestral state reconstruction provided no ro-
bust support for SSD in early sharks, with the ancestral values of
SD% and MFR overlapping with 0 and 1 respectively. This raises the
prospec t that SSD in extant selachimorphs is a derived state that
has evolved independently from SSD in other vertebrate lineages.
This remains to be empirically tested as palaeontological studies
of selachimorph taxa rarely comment on sexual size dimorphism.
However, given our finding that extant oviparous sharks exhibit
less SSD than matrotrophic species (Table 2) and the fact that ovi-
parity likely represents the ancestral reproductive mode in elasmo-
branchs (Katona et al., 2023), we hypothesise that any SSD found
in early selachimorphs would likely be relatively minor if present at
all. Subsequently, as alternative, matrotrophic reproductive modes
evolved in elasmobranchs, selection on increased female body size
was intensified, resulting in the evolution of female- biased SSD in
some lineages. We found that an OUM model of trait evolution best
explained the phylogenetic distribution of SSD in sharks (Table 1),
suggesting the presence of multiple adaptive peaks which may cor-
respond to male- biased and female- biased SSD. The adaptive nature
of both male and female- biased SSD is further evidenced by the fact
that both have evolved multiple times independently in extant spe-
cies (Figure 2). While it is evident that the evolution of female- biased
SSD in sharks was associated with the rise of matrotrophic repro-
ductive modes (Figure 2; Katona et al., 2023), the lack of any rela-
tionship between SSD and either ecology or sexual selection means
we are unable to speculate as to what selective forces have favoured
the repeated evolution of male- biased SSD. We must emphasise
that the evolutionary analyses we have utilised here have a number
of underlying assumptions and limitations, relying on phylogenetic
hypotheses and specific models of trait evolution. Further studies
incorporating additional proxies for sexual selection (both pre- and
post- copulatory) and resource partitioning will be necessar y to cate-
gorically rule out hypothesised drivers of male- biased SSD in sharks.
5 | CONCLUSIONS
SSD is undoubtedly abundant in nature, but there remains much con-
troversy over its adaptive value and the selective factors influenc-
ing its evolution. Overall, our analyses show that there is no uniform
relationship between selection and SSD across vertebrate phylogeny,
with superficially similar patterns of SSD in different lineages evolving
due to different combinations of selective pressures. It appears that
SSD is not ancestral to sharks and may have arisen initially due to the
evolution of matrotrophic reproductive modes. Certainly, there is a
trend in ex tant species, whereby oviparous taxa exhibit less, and more
male- biased SSD than matrotrophic taxa, with all available evidence
suggesting that this is due to selection on female body size induced by
matrotrophy itself, rather than sexual selection. The drivers of male-
biased SSD remain unknown and warrant further study. Sharks repre-
sent an important component of vertebrate diversity and occupy a key
phylogenetic position within jawed vertebrates, and thus these results
are of great importance to our understanding of the adaptive basis of
SSD, and how/why broad shifts in SSD trends and underlying drivers
may have occurred over vertebrate evolutionary histor y.
AUTHOR CONTRIBUTIONS
Joel H. Gayford: Conceptualization (lead); data curation (lead); for-
mal analysis (lead); writing – original draft (equal); writing – review
and editing (equal). Phillip C. Sternes: Conceptualization (support-
ing); data curation (supporting); writing – original draft (equal); writ-
ing – review and editing (equal).
ACKNOWLEDGEMENTS
The authors wish to thank Dr Lars Schmitz for providing valuable
comments and insight that helped refine this article.
FUNDING INFORMATION
The authors declare no funding for this study.
CONFLICT OF INTEREST STATEMENT
The authors declare no conflicts of interest regarding this study.
DATA AVAIL ABILI TY STATEMENT
All data generatedusedduringthisstudycanbefoundwithin the
article and associated Supporting Information.
ORCID
Joel H. Gay ford https://orcid.org/0000-0002-0839-3940
Phillip C . Sternes https://orcid.org/0000-0001-7223-3725
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How to cite this article: Gayford, J. H., & Sternes, P. C.
(2024). The origins and drivers of sexual size dimorphism in
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org /10.10 02/ece3.11163
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