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Males and females are often subjected to different selection pressures for homologous traits, resulting in sex-specific optima. Because organismal attributes usually share their genetic architectures, sex-specific selection may lead to intralocus sexual conflict. Evolution of sexual dimorphism may resolve this conflict, depending on the degree of cross-sex genetic correlation (rMF) and the strength of sex-specific selection. In theory, high rMF implies that sexes largely share the genetic base for a given trait and are consequently sexually monomorphic, while low rMF indicates a sex-specific genetic base and sexual dimorphism. Here, we broadly test this hypothesis on three spider species with varying degrees of female-biased sexual size dimorphism, Larinioides sclopetarius (sexual dimorphism index, SDI = 0.85), Nuctenea umbratica (SDI = 0.60), and Zygiella x-notata (SDI = 0.46). We assess rMF via same-sex and opposite-sex heritability estimates. We find moderate body mass heritability but no obvious patterns in sex-specific heritability. Against the prediction, the degree of sexual size dimorphism is unrelated to the relative strength of same-sex versus opposite-sex heritability. Our results do not support the hypothesis that sexual size dimorphism is negatively associated with rMF. We conclude that sex-specific genetic architecture may not be necessary for the evolution of a sexually dimorphic trait.
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ORIGINAL PAPER
Cross-sex genetic correlation does not extend to sexual size
dimorphism in spiders
Eva Turk
1
&MatjažKuntner
1,2,3,4
&Simona Kralj-Fišer
1,5
Received: 9 August 2017 / Revised: 23 November 2017 / Accepted: 27 November 2017
#Springer-Verlag GmbH Germany, part of Springer Nature 2017
Abstract
Males and females are often subjected to different selection pressures for homologous traits, resulting in sex-specific optima.
Because organismal attributes usually share their genetic architectures, sex-specific selection may lead to intralocus sexual
conflict. Evolution of sexual dimorphism may resolve this conflict, depending on the degree of cross-sex genetic correlation
(r
MF
) and the strength of sex-specific selection. In theory, high r
MF
implies that sexes largely share the genetic base for a given
trait and are consequently sexually monomorphic, while low r
MF
indicates a sex-specific genetic base and sexual dimorphism.
Here, we broadly test this hypothesis on three spider species with varying degrees of female-biased sexual size dimorphism,
Larinioides sclopetarius (sexual dimorphism index, SDI = 0.85), Nuctenea umbratica (SDI = 0.60), and Zygiella x-notata
(SDI = 0.46). We assess r
MF
via same-sex and opposite-sex heritability estimates. We find moderate body mass heritability but
no obvious patterns in sex-specific heritability. Against the prediction, the degree of sexual size dimorphism is unrelated to the
relative strength of same-sex versus opposite-sex heritability. Our results do not support the hypothesis that sexual size dimor-
phism is negatively associated with r
MF
. We conclude that sex-specificgenetic architecture may not be necessary for the evolution
of a sexually dimorphic trait.
Keywords Cross-sex genetic correlation .Trait evolution .Sexual dimorphism .Heritability .Sex-specific optimum .Pedigree
Introduction
In most sexualorganisms, both genders usually share the same
genetic architecture for homologous traits (Lande 1980).
When selection pressures on those traits are different in males
and females, sex-specific trait optima may arise. In extreme
cases, sex-specific selection acts in opposite ways, setting a
stage for intralocus sexual conflict. If unresolved, this conflict
prevents the sexes from achieving their respective trait optima,
resulting in sex-specific fitness reductions (Pennell and
Morrow 2013). Evolution of sexual dimorphism (SD) may
fully or partially resolve sexual conflict, depending on the
degree of cross-sex genetic correlation (r
MF
) for the trait and
the strength of sex-specific selection (Lande 1980).
Theoretically, high r
MF
should constrain the evolution of SD
and sustain sexual conflict. In other words, if r
MF
equals 1,
males and females are monomorphic due to near identical
genetic architecture for the trait. If, on the other hand, r
MF
is
close to zero, this would imply a sex-specific genetic base,
allowing for SD.
This scenario can be studied using trait heritability analysis.
r
MF
can be expressed as
Communicated by: Stano Pekar
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s00114-017-1529-6) contains supplementary
material, which is available to authorized users.
*Eva Turk
eva.turk@zrc-sazu.si
1
Institute of Biology, Research Centre of the Slovenian Academy of
Sciences and Arts, Ljubljana, Slovenia
2
Department of Entomology, National Museum of Natural History,
Smithsonian Institution, Washington, DC, USA
3
Centre for Behavioural Ecology and Evolution (CBEE), College of
Life Sciences, Hubei University, Wuhan, Hubei, China
4
National Institute of Biology, Ljubljana, Slovenia
5
Faculty of Mathematics, Natural Sciences and Information
Technologies, University of Primorska, Koper, Slovenia
The Science of Nature (2018) 105:1
https://doi.org/10.1007/s00114-017-1529-6
rMF ¼h2FD*h2MS
h2MD*h2FS

where h
2
represents narrow sense heritability estimates for all
possible parent-offspring combinations: father-daughter (FD),
mother-son (MS), mother-daughter (MD), and father-son (FS)
(Lynch and Walsh 1998). Narrow sense heritability is the pro-
portion of variance in a trait that is due to additive genetic
factors, calculated as the ratio of additive genetic variance to
total phenotypic variance (Lynch and Walsh 1998). Additive
genetic variance is an important parameter in quantitative ge-
netic research, because it implies the traits evolvability
(Falconer and Mackay 1996; Lynch and Walsh 1998).
Empirical studies that test the correlation between r
MF
and
SD yield mixed results, though generally confirm the expected
negative correlation (Poissant et al. 2010).
Body size is among the physical attributes of organisms
that influence most other aspects of their biology (Roff
1992), as it correlates closely with life-history traits in verte-
brates and invertebrates (Peters 1983;Honěk1993). Body size
notably affects individualsperformance in foraging, as well
as juvenile development time and longevity (Kessler 1971;
Simpson 1995). In females, body size influences fecundity,
larger females producing more offspring (Kessler 1971; Fritz
and Morse 1985; Gonzaga and Vasconcellos-Neto 2001;
Branson 2008). On the other hand, male body size influences
performance in direct and indirect male-male competition
(Rosenberg and Enquist 1991). Due to sex-specific selection
pressures, the optimal body size may differ for males and
females, resulting in sexual size dimorphism (SSD;
Blanckenhorn 2005).
Spiders are known for female-biased SSD, in some cases so
extreme that females weigh 125 times more than males
(Kuntner et al. 2012; Cheng and Kuntner 2014). While studies
agree that female body size in spiders strongly responds to
fecundity selection (Head 1995; Reeve and Fairbairn 1996),
it is less clear what selection pressures act on males (Kuntner
and Elgar 2014). For example, scramble competition, gravity,
sexual cannibalism, and mortality are all believed to select for
small male size, while male-male competition favors large
males (Elgar 1991; Moya-Laraño et al. 2002;Maklakov
et al. 2004; Blanckenhorn 2005; Foellmer and Fairbairn
2005; Kasumovic et al. 2006; Kasumovic and Andrade
2009; Danielson-François et al. 2012; Kuntner and Elgar
2014). These diverse, sex-specific selection pressures along
with a large range of spider SSD make spiders suitable organ-
isms for the study of the relationship between size heritability
and SSD.
Here, we explore body mass heritability in three species of
orb-web spiders exhibiting varying degrees of female-biased
SSD: bridge spider (Larinioides sclopetarius), walnut orb-
weaver (Nuctenea umbratica), and silver-sided sector spider
(Zygiella x-notata). Using a fixed size parameter, such as car-
apace width, provides the optimal size proxy for quantitative
genetic studies, as it is largely independent of individual body
condition and does not change after maturation. However, as
we explain in the methods, we use body mass as a proxy for
body size, because these two parameters strongly correlate in
invertebrates, including spiders (Honěk1993; Legaspi and
Legaspi 2005; Branson 2008; Neumann and Schneider 2015).
Data on body mass, combined with a record of the individ-
ualspedigrees, enable the estimation of body mass heritabil-
ity and calculation of r
MF
.Wepredictr
MF
to be higher in more
size monomorphic and lower in more size dimorphic species.
When body size is a strongly sexually dimorphic trait, the
degree of same-sex size heritability is expected to be high
and the degree of opposite-sex size heritability low. On the
other hand, more size monomorphic species are expected to
exhibit similar degrees of heritability from both parents. In
other words, we predict to detect relatively higher h
2
MD
and
h
2
FS
and lower h
2
FD
and h
2
MS
when SSD is high.
Material and methods
Studied species
We chose three species of spiders that are easily accessible and
collectable in the field in Slovenia. They all belong to the same
family: the classical orb-web spiders (Araneidae). While we
acknowledge that Larinioides and Nuctenea are much more
closely related than either is to Zygiella (Gregoričet al. 2015),
this study aims at comparing araneids with similar life histo-
ries and varying degrees of SSD.
The bridge spider, Larinioides sclopetarius (Clerck 1757),
is a common Holarctic species. High density populations
consisting of individuals of both sexes and different ages col-
onize urban constructions near bodies of water (Heiling and
Herberstein 1998). Bridge spiders exhibit a pronounced,
female-biased SSD. Females have a longer developmental
time than malesunder a high feeding regime, males mature,
on average, 26 days earlier than do females (Kleinteich and
Schneider 2010). While females build, maintain, and defend
their webs, males live kleptoparasitically on the femaleswebs
(Heiling and Herberstein 1998). Prior laboratory studies found
that L. sclopetarius exhibit high developmental plasticity de-
pending on foodavailability, a short life cycle of about 60 days
at ample food, and high reproductive output of up to 12 viable
egg cases (Kleinteich and Schneider 2011; own data).
The silver-sided sector spider, Zygiella x-notata (Clerck
1757), is also a common Holarctic species that often inhabits
human constructions such as walls, fences, and window
frames but can also inhabit urban or pristine vegetation
(Leborgne and Pasquet 1987). Zygiella x-notata females are
moderately larger than their male conspecifics and need
1 Page 2 of 8 Sci Nat (2018) 105:1
approximately 14 days longer time to reach maturity (Mayntz
et al. 2003). They exhibit developmental plasticity depended
on food availability, have an intermediate developmental time
of 160 days at ample food (Mayntz et al. 2003), and a repro-
ductive output of up to eight viable egg cases (own data).
The walnut orb-weaver, Nuctenea umbratica (Clerck
1757), is a common central European species. It prefers land-
scapes with semi-open habitats, such as forest edge, hedge-
rows, orchards, and single trees (Horváth and Szinetár 2002;
Horváth et al. 2005; Bucher et al. 2010). Females are larger
than males and develop more slowly (Kralj-Fišer et al. 2014).
Its female-biased SSD is intermediate among the three studied
species. If well fed, males mature on average 30 days earlier
than females (Kralj-Fišer et al. 2014). In comparison to the
previous two species, N. umbratica development is more can-
alized, meaning that spidersphenotype is similar regardless
of food availability. In comparison to other two species, the
walnut orb-weaver exhibits a long life cycle (240 days at am-
ple food) and a low reproductive output of up to four viable
egg cases (Kralj-Fišer et al. 2014; own data).
Field collection
Subadult males and females were collected in the field and
transferred to the laboratory to be reared to maturity.
Larinioides sclopetarius were collected from buildings,
fences, and bridges along riverbanks in Hamburg, Germany
(53.577401, 10.009699), in September 2010. Zygiella x-
notata were collected from man-made constructions along
the Vipava riverbank, Slovenia (45.844605, 13.963604), in
May 2012. Nuctenea umbratica were collected from their
webs on trees and hedgerows along the Ljubljanica riverbank,
Slovenia (46.045093, 14.506048), between May and
July 2011.
Laboratory rearing and data collection
Field-collected spiders were reared under standardized labo-
ratory conditions (room temperature, L/D = 10:14). They were
kept in 200-ml plastic cups and fed ad libitum with fruit flies
(Drosophila sp.) until the final molt. Upon maturation, fe-
males were relocated into plastic frames (36 × 36 × 6 cm)
andfedtwoblowflies(Calliphora sp.)twiceaweek.
Because adult males cease to construct webs, they were left
in the original plastic cups, subjected to the same feeding
treatment as females. Throughout the study, the spiders were
water-sprayed 5 days a week to maintain humidity. At matu-
rity and while still virgin, all spiders were weighed (accuracy
of 0.01 mg). We measured 59 L. sclopetarius spiders (Nfe-
males = 29, Nmales = 30; age at weighing = 8.5 ± 7.25 days),
53 Z. x-notata spiders (Nfemales = 29, Nmales = 24; age at
weighing = 28.28 ± 16.09 days), and 95 N. umbratica spiders
(Nfemales = 41, Nmales = 54; age at weighing = 1.04 ±
0.41 days).
All spiders were then used for studies of assortative mating
(Kralj-Fišer and Schneider 2012;Kralj-Fišer et al. 2017).
Males and females were mated according to their aggressive-
ness score; however, aggressiveness did not show any corre-
lation with body mass (Kralj-Fišer and Schneider 2012),
meaning that spiders were mated randomly in respect to body
mass. We initiated mating encounters that lasted24 h (to allow
time for successful mating) by placing a male on a females
web with a paintbrush. We then separated the couples and
continued rearing the spiders individually until their natural
death. We monitored the frames for deposited egg cases,
which we collected and stored at room temperature until
hatching. After the second molt, we placed a subset of
spiderlings from each parental pair into individual 200 ml
plastic cups to be reared under standardized conditions.
Upon molting to adulthood and while still virgin, we weighed
the spiders like those of the parental generation. In
L. sclopetarius, we weighed five male and five female off-
spring per family, i.e., parental pair (Nfamilies = 29). In
strongly sex-biased clutches, the data thus include fewer than
ten spiders. In Z. x-notata (Nfamilies = 29) and N. umbratica
(Nfamilies = 41), we weighed three males and three females
per family. In the offspring generation, we measured a total of
269 L. sclopetarius spiders (Nfemales = 134, Nmales = 125;
age at weighing = 6.35 ± 6.56 days), 132 Z. x-notata spiders
(Nfemales = 63, Nmales = 69; age at weighing = 16.59 ±
7.80 days), and 90 N. umbratica spiders (Nfemales = 46, N
males = 44; age at weighing = 47.33 ± 20.83 days).
Spiders from the offspring generation were used for further
experiments (Kralj-Fišer and Schneider 2012), during which
many were cannibalized. The rest were not preserved in eth-
anol, because identification markings made on the spiders
wore off during the experiments, and individual recognition
of the surviving spiders was no longer possible. Fixed size
data could not be reliably obtained, so we used body mass
as a proxy for body size. Female spiders of all three species
showed significant weight gain with age (own data). We
accounted for this using ordinary least squares regression in
SDI calculations and by including age as a covariate in
MCMCglmm analyses.
Statistical analyses
We used the size dimorphism index (SDI; Lovich and
Gibbons 1992) to quantify SSD, pooling data for both gener-
ations for each species:
SDI ¼females0mean mass
males0mean mass
1
Sci Nat (2018) 105:1 Page 3 of 8 1
This SDI includes the subtraction of 1 if females are the
larger sex, in order to achieve directionality of the index.
Consequently, the resulting index only reflects the true pro-
portion of SSD after the addition of 1 (Lovich and Gibbons
1992).
We calculated estimates of body mass heritability follow-
ing Wilson et al. (2010) and de Villemereuil (2012),
performing Markov Chain Monte Carlo linear mixed model
(MCMCglmm) analyses in R (version 2.15.3, R Core Team
2013;Hadfield2010). We ran the protocol using two priors,
differing in the assumed ratio between residual and genetic
variance in body mass. The first assumes all variance is either
residual or genetic, and the second assumes half of the total
variance to eachcomponent (shown in Appendices S1 and S2,
respectively). Using the first prior resulted in a greater effec-
tive sample size and was thus used for further analyses.
In order to define relatedness between individuals, a pedi-
gree was constructed, containing each individual included in
the analysis. Individuals of the parental generation were field-
collected and their family tree is unknown, so their parents
were marked with N/A. Heritability estimates were then cal-
culated for every parent-offspring combination for each spe-
cies, with sex and age at weighing as covariates and pedigree
as a random factor. Appendix S1 lists the full R script used in
the analyses. Cross-sex genetic correlation (r
MF
) was assessed
for each species after Lynch and Walsh (1998).
The model we used is relatively general, because sample
sizes proved much too small to work with more complex
models. We ran a complex model that accounted for sibling
covariation; however, the resulting credible intervals were ex-
tremely wide suggesting very high uncertainty. Accurate r
MF
estimations using such a model would require sample sizes of
thousands of individuals from hundreds of families (Hadfield,
personal communication).
Results
In all three species, females were heavier than males (for av-
erage body mass with standard deviation for each species, see
Tab le 1; for error bars of average body mass with confidence
intervals by sex, generation, and species, see Fig. 1).
Larinioides sclopetarius was the most size dimorphic
(SDI = 0.847), Z. x-notata the least (SDI = 0.462), and
N. umbratica was moderately size dimorphic (SDI = 0.597).
This is also visible from Fig. 1, where the difference between
femaleandmalemeanbodymassisthebiggestin
L. sclopetarius and the smallest in Z. x-notata.
We found moderate heritability of body mass in all three
species (L. sclopetarius,h
2
=0.208;N. umbratica,h
2
=0.210;
Z. x-notata,h
2
=0.390; Table 2) when pooling all data.
Maternal heritability estimates were 0.311 in L. sclopetarius,
0.234 in N. umbratica, and 0.538 in Z. x-notata (Table 2).
Paternal heritability estimates were 0.402, 0.283, and 0.481
in L. sclopetarius,N. umbratica,andZ. x-notata,respectively
(Table 2).
Against our prediction, in the most size dimorphic species
L. sclopetarius, mean heritability estimates for same-sex com-
binations (h
2
MD
=0.300,h
2
FS
= 0.350) were lower than mean
heritability estimates for opposite-sex combinations (h
2
MS
=
0.484, h
2
FD
= 0.410; Table 2). In N. umbratica, daughters
have higher mean heritability estimates than sons through
both parents; mean h
2
MD
was higher than mean h
2
MS
,while
mean h
2
FD
was higher than mean h
2
FS
(h
2
MD
=0.453,h
2
FS
=
0.291, h
2
MS
=0.241,h
2
FD
= 0.465; Table 2). Mean heritability
estimates in Z. x-notata were similar and high when estimated
through fathers and mothers with somewhat higher mean her-
itability estimates to daughters than sons (h
2
MD
= 0.472,
h
2
FS
=0.587,h
2
MS
=0.572, h
2
FD
= 0.517; Table 2). It should
be noted that in all three species, credible intervals for all four
heritability combinations largely overlap (Table 2).
In contrast to our prediction that cross-sex genetic correla-
tion would be lower in more size-dimorphic species, r
MF
es-
timates in the tested species were all close to 1: L. sclopetarius
(r
MF
= 1.375), N. umbratica (r
MF
= 0.922), and Z. x-notata
(r
MF
=1.033).
Discussion
The evolution of sexual dimorphism is frequently explained
by low cross-sex genetic correlation (r
MF
< < 1), which would
allow both sexes to evolve their respective optimal pheno-
types (Lande 1980). Considering body size or mass, low
cross-sex genetic correlation should be more typical of sexu-
ally size dimorphic rather than monomorphic species. We
tested this hypothesis in three orb-web spider species with
body mass sexual dimorphism indices (SDI) of 0.85
(L. sclopetarius), 0.60 (N. umbratica), and 0.46 (Z. x-notata),
predicting that cross-sex genetic correlation would be lowest
in L. sclopetarius and highest in Z. x-notata. Contrary to this
prediction, we found comparably high cross-sex genetic cor-
relation in all three species. Our results refute a clear relation-
ship between the level of SDI and r
MF
.
We detect no sex-specific heritability pattern of body mass
in any species. When looking at general, cross-population
body mass heritability from pooled data, L. sclopetarius
(0.21) and N. umbratica (0.22) exhibit a moderate influence
of additive genetic factors on body mass, while this influence
is somewhat higher in Z. x-notata (0.39).In comparison, mass
heritability is estimated between 0.37 and 0.65 in the seed
beetle Callosobruchus maculatus (Fabricius 1775) (Fox
et al. 2004a), 0.48 in the moth Utetheisa ornatrix (Linnaeus
1758) (Iyengar and Eisner 1999), and 0.6 in the cellar spider
Pholcus phalangioides (Füssli 1775) (Uhl et al. 2004). Our
detected heritability values are lower compared to those
1 Page 4 of 8 Sci Nat (2018) 105:1
above. It may be worth noting that the species we studied
show higher female-biased SSD.
In theory, sex-specific selection should lead to greater her-
itability between same-sex individuals than opposite-sex indi-
viduals (Bonduriansky and Rowe 2005a). Female offspring
should be more likely to inherit alleles that benefit female
fitness from their mothers than from their fathers, which are
not subjected to sexual selection for that trait (Bonduriansky
and Rowe 2005a). Our results, however, do not adhere to this
predicted pattern. A possible proximate explanation for the
observed deviation from the hypothetical pattern of heritabil-
ity is the existence of parent-of-origin influence on gene ex-
pression, also known as genomic imprinting (Day and
Bonduriansky 2004; Bonduriansky and Chenoweth 2009).
Our study did not test for effects of genomic imprinting, so
further analyses would be needed to confirm its influence.
Importantly, existing studies of heritability in animals are
largely restricted to laboratory-kept populations. Arguably,
heritability estimates in laboratory populations under con-
trolled conditions tend to be greater than in natural popula-
tions (Riska et al. 1989). However, a major problem with the
study of wild populations is the construction of a pedigree,
essential in heritability studies (Lynch and Walsh 1998). Our
study constructs the offspring (though not the parental) pedi-
gree and standardizes the environmental factors influencing
the offspring, which may be reflected in narrower 95% confi-
dence intervals in the offspring generation compared to the
parental (Fig. 1). In summation, our body mass heritability
estimates could be lower due to such methodological differ-
ences in comparison to studies on solely laboratory-kept
populations.
We fail to support our prediction that cross-genetic corre-
lations for body mass will be significantly lower than 1 in all
three species, with r
MF
being the highest in the species with
the lowest SDI and vice-versa. Contrary to our expectations,
all three r
MF
estimates in the tested species were close to 1.
Our estimated values for r
MF
resemble those for size mono-
morphic arthropods (cellar spider P. phalangioides, SDI =
0.07, r
MF
=0.94,Uhl etal.2004; black tiger prawn Penaeus
monodon (Fabricius 1798), SDI = 0.09, r
MF
=0.97, Kenway
et al. 2006; black field cricket Teleogryllus commodus (Walker
1869), SDI not listed, r
MF
= 0.96, Zajitschek et al. 2007).
Fig. 1 Mean body mass of males
and females in parental (upper
panels) and offspring (lower
panels) generations of the three
study species. Whiskers are 95%
confidence intervals
Table 1 Average body mas s ±
95% standard deviation by sex
and sexual dimorphism indices
calculated from pooled data for
each species
Female body mass average
(grams)
Male body mass average
(grams)
Sexual dimorphism index
(SDI)
L. sclopetarius 0.109 ± 0.043 0.059 ± 0.012 0.847
N. umbratica 0.107 ± 0.030 0.067 ± 0.021 0.597
Z. x-notata 0.038 ± 0.012 0.026 ± 0.006 0.462
Sci Nat (2018) 105:1 Page 5 of 8 1
For a relevant comparison, one needs to parallel our study
to those on invertebrate species with SDI scores over 0.4. To
list some examples, eye span to body length ratio in the stalk-
eyed fly (Cyrtodiopsis dalmanni (Wiedemann 1830), SD =
0.41) shows a cross-genetic correlation of 0.29 (Wilkinson
1993), while antenna length in the waltzing fly (Prochyliza
xanthostoma (Walker 1849), SD = 0.62) shows a cross-
genetic correlation of 0.21 (Bonduriansky and Rowe 2005b).
In water striders (Aquarius remiges (Say 1832), SDI = 0.7),
however, r
MF
estimates range from 0.17 (mid-femur length)
to 1.01 (abdomen length) (Preziosi and Roff 1998). In general,
a negative relationship between SDI and r
MF
does exist
(Poissant et al. 2010), but there are several examples that do
not conform to the rule.
A wide range of cross-sex genetic correlation scores has
been found across several studies of sexual size dimorphism,
both in and among populations. For instance, the cross-sex
genetic correlation for body mass differed substantially
between two populations of the seed beetle C. maculatus
(south India: r
MF
= 0.28, Burkina Faso: r
MF
=0.91,Fox etal.
2004a). In other words, the two populations differed in the
genetic basis for sexual dimorphism. The reasons behind this
are not fully understood, but several possible contributing fac-
tors have been proposed. Fox et al. (2004b) stress the impor-
tance of non-additive genetic factors (gene interactions), such
as dominance and epistasis, and the maternal effect.
Additionally, heritability estimates may be influenced by the
so-called common environment effect, which attributes simi-
larity between organisms to the common environment in
which they live, rather than their genetic makeup (Roff
1997; Uhl et al. 2004). The actual influence of non-additive
genetic factors and maternal effect on offspring fitness re-
mains unclear and was not controlled for in the present study,
while the effect of a common environment was minimized by
keeping each spider in its own container.
To recap the theory, when selection acts in sex-specific
directions, the evolution of sexual dimorphism should be fa-
cilitated by low r
MF
values (Lande 1980). However, several
scenarios may account for a pronounced SSD in the absence
of clear sex-specific genotypes. First, model simulations by
Reeve and Fairbairn (2001) allow for evolution of sexual di-
morphism even while maintaining relatively high r
MF
,ifonly
allele frequencies change, rather than the genetic architecture
as a whole. This suggests that high r
MF
can point to either
sexual monomorphism or sexual dimorphism with a resolved
intralocus sexual conflict (Bonduriansky and Chenoweth
2009). Therefore, it may be that in our tested species,
intralocus sexual conflict is resolved through allele frequency
shifts rather than changes in genetic makeup. Alternatively,
sex-specific gene expression may underlie high SSD despite
a genetic base shared between males and females. These sce-
narios require quantitative genetic or transcriptomic tests in
species with varying degrees of SSD.
The unexpectedly high r
MF
scores likewise require a meth-
odological clarification. The r
MF
equation (Lynch and Walsh
1998) assumes heritability to be higher in same-sex (mother-
daughter, father-son) than opposite-sex pairings (mother-son,
father-daughter). If that is true, the resulting correlation value
must fall within the mathematically logical range of values
between 0 and 1. However, the biological reality based on
our results is that opposite-sex pairings may have higher
heritability values than same-sex pairings. Consequently, the
numerator is greater than the denominator and the resulting
value exceeds 1 (also see Reeve and Fairbairn 2001). Thus,
values above 1 may be valid and are indeed common in r
MF
studies (Preziosi and Roff 1998;Foxetal.2004a;
Bonduriansky and Rowe 2005a).
We need to acknowledge the drawbacks of this study. Its
foremost weakness is the use of body mass as a proxy for body
size, for reasons explained in the methods. Additionally,
sample sizes could be increased, allowing for more complex
Table 2 Heritability estimates
and 95% credible intervals (Cred.
int.) for every parent-offspring
combination in each species
Mothers Cred. int. Fathers Cred. int. All parents Cred. int.
Larinioides sclopetarius (N=318)
Daughters 0.300 0.1100.530 0.410 0.1660.670 0.227 0.0910.379
Sons 0.484 0.2810.710 0.350 0.1230.584 0.411 0.2460.581
All offspring 0.311 0.1300.521 0.402 0.2040.610 0.208 0.1070.311
Nuctenea umbratica (N=181)
Daughters 0.453 0.2200.722 0.465 0.2600.686 0.369 0.1820.563
Sons 0.241 0.0780.444 0.291 0.0740.521 0.196 0.0740.347
All offspring 0.234 0.0910.407 0.283 0.0970.505 0.210 0.0840.348
Zygiella x-notata (N=185)
Daughters 0.472 0.1490.815 0.517 0.2440.798 0.387 0.1520.640
Sons 0.572 0.2820.844 0.587 0.2800.895 0.497 0.2360.746
All offspring 0.538 0.2640.807 0.481 0.2480.722 0.390 0.1810.600
1 Page 6 of 8 Sci Nat (2018) 105:1
statistical analyses. As suggested by Hadfield (personal com-
munication), we would need thousands of individuals for re-
liable r
MF
analyses using complex MCMCglmm protocols.
However, quantitative genetic studies on a wide range of di-
verse species are needed for a general understanding of trait
heritability and the evolution of SSD in spiders and we trust
this study is a valuable contribution towards that aim.
In conclusion, our findings do not support the hypothesis
that SSD is negatively correlated with cross-sex genetic cor-
relation if assessed via same-sex and opposite-sex heritability
estimates. It seems that a sex-specific genetic architecture is
not necessary for the evolution of a sexually dimorphic trait.
Acknowledgments We thank Tomma Dirks, Angelika Tabel-Hellwig,
Rebeka Šiling, Tjaša Lokovšek, and Klavdija Šuen for the spider hus-
bandry and Klemen Čandek and MatjažGregoričfor the help with field
work. SKF was granted a Humboldt Postdoctoral Fellowship, a
Humboldt Return Fellowship, and was supported by the Slovenian
Research Agency (grant Z1-4194); MK was supported by the Slovenian
Research Agency (grants P1-10236 and J1-6729). All data analyzed dur-
ing this study are included in this published article and its supplementary
information file.
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... Previous studies in spiders with moderate SSD show body size to be only moderately heritable (h 2 ~ 0.20-0.39; Turk, Kuntner, and Kralj-Fišer 2018) suggesting considerable plasticity in body size. This plasticity can also be lineage-specific (e.g. ...
... However, our results from the general linear mixed models clearly show that male offspring mass at maturation does not correlate to sire mass (Fig. 4). A study on cross-sex genetic correlation of size for other orb-weavers suggests a rather equal sex contribution to size regardless of the degree of SSD (Turk et al. 2018). However, their subject species did not exhibit extreme SSD, and therefore future quantitative genetic studies will help better establish the genetic architecture and heritability patterns of body size in extreme SSD species. ...
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Behavioral characteristics importantly shape an animals’ ability to adapt to changing conditions. The notion that behavioral flexibility facilitates exploitation of urban environments has received mixed support, but recent studies propose that between-individual differences are important. We leverage existing knowledge on three species of orb-web spider (Araneidae, Araneae) whose abundances differ along an urban–rural gradient to test predictions about between- and within-species/individual behavioral variation. We sampled Larinioides sclopetarius from their urban environment, and two species from suburban environments, Zygiella x-notata and Nuctenea umbratica. For each species, we quantified activity in a novel environment and within-species aggression. We analyzed between- and within-individual variation in behavior as well as their repeatability and correlations. As predicted, L. sclopetarius exhibited the highest activity in a novel environment and N. umbratica the lowest. Across all species, males were more aggressive than females and Z. x-notata was the most aggressive, followed by L. sclopetarius and N. umbratica. For all species, between-individual differences in activity and aggressiveness were repeatable; but the two behaviors were not correlated for any species. We next tested how group composition in relation to aggressiveness affects survival in high density conditions. Groups of Z. x-notata consisting of aggressive and tolerant spiders had higher survival rates than groups composed of only aggressive or tolerant individuals. Ultimately, we uncovered a complex pattern of behavioral variation between species as well as between and within individuals and we discuss the relative roles of this variation with respect to adapting to urban environments. Significance statement Urbanization has drastically changed biodiversity patterns. While the majority of species cope poorly with urban habitats, some species flourish in cities. Our understanding of behavioral characteristics that facilitate this exploitation, however, remains poor. We explored between and within species and individual variation in behaviors in ecologically similar orb-weaving spider species whose abundances differ along the urban–rural gradient. We detect both consistent individual differences and plasticity, in individuals’ response to a novel environment, suggesting that some degree of flexibility in reaction to novelty may be crucial in an urbanized environment. We also found that variation in aggressiveness type enables survival in high density conditions, conditions typical for urban populations. Urban populations thus exhibit a complex pattern of behavioral flexibility and behavioral stability.
Chapter
Age and size at maturity have been an object of interest to humans since the domestication of animals and plants, for one of the objectives of domestication was to produce an organism that grew fast and matured early at a large size. Selection was also practiced to produce animals that could be used for such purposes as hunting and portaging, and to produce products for pleasure alone, as seen in the many ornamental varieties of dogs, cats, goldfish, pigeons, and plants. All of these instances demonstrate that age and size at maturity are traits that are relatively easily molded by artificial selection and, by extension, natural selection. Historically, artificial selection experiments were concerned not with the evolution of age and size at maturity in natural populations but with the production of economically more valuable plants and animals. Recently, there has been a substantial increase in the quantitative genetic analysis of nondomesticated organisms, which has shown that, with respect to morphological traits such as adult size, there is typically abundant additive genetic variance, with heritabilities averaging approximately 0.4 (reviewed in Roff 1997). Life history traits, such as the age at maturity, show, on average, lower heritabilities (approx. 0.26) but still enough for rapid evolutionary change. Quantitative genetic analyses have shown that age and size at maturity can evolve, but the most significant advances in our understanding of the factors favoring particular age at maturity/body size combinations are due to mathematical models predicated upon the assumption that selection maximizes some fitness measure such as the rate of increase, r. In a paper entitled “Adaptive Significance of Large Size and Long Life of the Chaetognath Sagitta elegans in the Arctic,” McLaren (1966) produced a seminal analysis in which he incorporated all the important elements that have appeared in subsequent analyses of the evolution of age and size at maturity. Specifically, McLaren attempted to take into account the trade-offs produced by increased fecundity being bought at the expense of delayed maturity and increased mortality. In this chapter, I shall primarily consider analyses that have followed in McLaren’s footsteps.
Article
We artificially selected for body size in Drosophila melanogaster to test Lande's quantitative genetic model for the evolution of sexual size dimorphism. Thorax width was used as an estimator of body size. Selection was maintained for 21 generations in both directions on males only, females only, or both sexes simultaneously. The correlated response of sexual size dimorphism in each selection regime was compared to the response predicted by four variants of the model, each of which differed only in assumptions about input parameters. Body size responded well to selection, but the correlated response of sexual size dimorphism was weaker than that predicted by any of the variants. Dimorphism decreased in most selection lines, contrary to the model predictions. We suggest that selection on body size acts primarily on growth trajectories. Changes in dimorphism are caused by the fact that male and female growth trajectories are not parallel and termination of growth at different points along the curves results in dimorphism levels that are difficult to predict without detailed knowledge of growth parameters. This may also explain many of the inconsistent results in dimorphism changes seen in earlier selection experiments.
Chapter
The last chapter examined the genetic basis of the resemblance between parents and offspring for a single trait. However, it is common experience that traits are not inherited as independent units, but that several traits tend to be associated with each other. This phenomenon can arise in two ways: first, a subset of the genes that influence one trait may also influence another trait, a phenomenon known as pleiotropy, and second, the genes may act independently on the two traits, but because of nonrandom mating, selection, or drift they may be associated, a phenomenon called linkage disequilibrium. The latter causes only a transitory association between traits and it is the former which is of greatest interest to evolutionary biologists for pleiotropic effects may greatly alter the rate and direction of evolution. This is discussed in greater detail in Chapter 5. The present CHAPTER is concerned with the theory of the genetic correlation, its estimation, and the comparison of genetic correlations among populations.