Sex-specific developmental trajectories in an extremely sexually size dimorphic spider

Abstract

Adult body size, development time, and growth rates are components of organismal life histories, which crucially influence fitness and are subject to trade-offs. If selection is sex-specific, male and female developments can eventually lead to different optimal sizes. This can be achieved through developmental plasticity and sex-specific developmental trajectories. Spiders present suitable animals to study differences in developmental plasticity and life history trade-offs between the sexes, because of their pronounced sexual dimorphism. Here, we examine variation in life histories in the extremely sexually size dimorphic African hermit spider (Nephilingis cruentata) reared under standardized laboratory conditions. Females average 70 times greater body mass (and greater body size) at maturity than males, which they achieve by developing longer and growing faster. We find a small to moderate amount of variability in life history traits to be caused by family effects, comprising genetic, maternal, and early common environmental effects, suggesting considerable plasticity in life histories. Remarkably, family effects explain a higher variance in male compared to female life histories, implying that female developmental trajectories may be more responsive to environment. We also find sex differences in life history trade-offs and show that males with longer development times grow larger but exhibit shorter adult longevity. Female developmental time also correlates positively with adult body mass, but the trade-offs between female adult mass, reproduction, and longevity are less clear. We discuss the implications of these findings in the light of evolutionary trade-offs between life history traits.

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https://doi.org/10.1007/s00114-021-01754-w
ORIGINAL ARTICLE
Sex‑specific developmental trajectories inanextremely sexually size
dimorphic spider
JankoŠet1· EvaTurk1· RokGolobinek1· TjašaLokovšek1· MatjažGregorič1· ShakiraGuaníQuiñonesLebrón1·
MatjažKuntner1,2· CharlesR.Haddad3· KlemenČandek2· SimonaKralj‑Fišer1
Received: 22 June 2021 / Revised: 6 August 2021 / Accepted: 1 September 2021
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021
Abstract
Adult body size, development time, and growth rates are components of organismal life histories, which crucially influ-
ence fitness and are subject to trade-offs. If selection is sex-specific, male and female developments can eventually lead to
different optimal sizes. This can be achieved through developmental plasticity and sex-specific developmental trajectories.
Spiders present suitable animals to study differences in developmental plasticity and life history trade-offs between the sexes,
because of their pronounced sexual dimorphism. Here, we examine variation in life histories in the extremely sexually size
dimorphic African hermit spider (Nephilingis cruentata) reared under standardized laboratory conditions. Females aver-
age 70 times greater body mass (and greater body size) at maturity than males, which they achieve by developing longer
and growing faster. We find a small to moderate amount of variability in life history traits to be caused by family effects,
comprising genetic, maternal, and early common environmental effects, suggesting considerable plasticity in life histories.
Remarkably, family effects explain a higher variance in male compared to female life histories, implying that female devel-
opmental trajectories may be more responsive to environment. We also find sex differences in life history trade-offs and
show that males with longer development times grow larger but exhibit shorter adult longevity. Female developmental time
also correlates positively with adult body mass, but the trade-offs between female adult mass, reproduction, and longevity
are less clear. We discuss the implications of these findings in the light of evolutionary trade-offs between life history traits.
Keywords Sexual dimorphism· Developmental plasticity· Body size· Sexual selection· Life history trade-off
Introduction
Life history traits such as adult body size, developmental
time, and growth rate play an important role in individual
fitness (Roff 1992; Stearns 1992). Life histories evolve
in response to selection within the constraints set by the
trade-off in their effects on fitness (Partridge and Sibly
1991). In theory, larger body sizes in animals ensure higher
fecundity, survival, and mating success (Blanckenhorn
2000), while smaller body sizes, resulting from shorter
development times, enable earlier maturation, increased sur-
vival prior to reproduction, and facilitate early or prolonged
access to resources, including mates (Roff 1992; Zonneveld
1996). Large body size and long development often corre-
late, generating a trade-off between the two traits (Roff 1992;
Nylin and Gotthard 1998).
While body size in female arthropods and other ecto-
therms commonly positively correlates with fecundity
(Honěk 1993; Head 1995), the evolution of male size
appears more complex. Large males could have an advantage
in male–male competition (Christenson and Goist 1979),
mate choice (Gilburn and Day 1994), and sperm competi-
tion (Kralj-Fišer etal. 2013), whereas small male sizes may
enhance mobility (Corcobado etal. 2010; but see Quiñones-
Lebrón etal. 2019) and the ability to find mates (Tammaru
Communicated by: José Eduardo Serrão.
Janko Šet, and Eva Turk are equal contribution
* Simona Kralj-Fišer
simonakf@zrc-sazu.si
1 Institute ofBiology, Research Centre oftheSlovenian
Academy ofSciences andArts, Ljubljana, Slovenia
2 Department ofOrganisms andEcosystems Research,
Evolutionary Zoology Laboratory, National Institute
ofBiology, Ljubljana, Slovenia
3 Department ofZoology & Entomology, University
oftheFree State, Bloemfontein, SouthAfrica

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etal. 1996). However, when male size is not a critical factor
in mating success, growth to the minimal size necessary to
sustain gonad development and ensure success in scramble
competition for mates is the stable life history strategy (Roff
1992; Quiñones-Lebrón etal. 2021).
Development time dictates when and at what size an
individual reaches adulthood and starts to reproduce (Roff
1992; Stearns 1992). While longer development leads to
advantages linked to larger body sizes, it also increases the
chance of juvenile mortality, shortens reproductive time, and
consequently limits mate availability, which leads to a trade-
off between development time and body size at maturation
(Roff 1992; Stearns 1992). Theory predicts that in arthro-
pods, selection favours females growing larger to maximize
fecundity (i.e. the fecundity hypothesis), while males are
selected for shorter development, potentially leading to pro-
tandry (small, early males) and sexual size dimorphism (late,
large females) (Singer 1982; Zonneveld 1996; Foellmer and
Moya-Laraño 2007).
Variation in life history traits within a population results
from the variability of genetic, maternal, and environmental
factors (Roff 2012). Narrow-sense heritability of life his-
tory traits, defining how much phenotypic variability in the
population is explained by the variation in additive genetic
effects, has been estimated to average 21% across animal
groups (Moore etal. 2019). Maternal effects, i.e. maternal
phenotype’s causal influence on the phenotype of her off-
spring (Bernardo 1996), explain approximately 11% of vari-
ation in life histories across animals (Moore etal. 2019).
This implies that high variability in life histories may be
a consequence of phenotypic plasticity, i.e. the ability of
a single genotype to produce alternative phenotypes in
response to environmental conditions (West-Eberhard 2003).
In arthropods, developmental plasticity can be induced by
environmental variables such as diet quality or quantity
(Esperk etal. 2007; Kralj-Fišer etal. 2014), temperature (Li
and Jackson 1996; Stillwell and Fox 2009), and photoperiod
(Schaefer 1977; Leimar 1996).
The degree of developmental plasticity may differ substan-
tially between the sexes (reviewed in Stillwell etal. 2010).
Several adaptive hypotheses have been proposed to explain
this pattern. The adaptive canalization hypothesis predicts the
least plasticity in traits under the strongest directional selec-
tion (Fairbairn 2005), while the condition dependence hypoth-
esis predicts the greatest plasticity in traits under the strongest
balancing selection (Bonduriansky 2007). Only a few studies,
however, have empirically tested them (e.g.Fairbairn 2005;
Fernández-Montraveta and Moya-Laraño 2007; Stillwell and
Fox 2009).
Spiders make ideal subjects for studying intersexual dif-
ferences in developmental trajectories and life history trade-
offs. Many spiders are sexually size dimorphic, with females
often considerably larger than males, in extremes up to 500
times heavier than males (Kuntner and Coddington 2020).
Furthermore, spiders have discrete and terminate growth
— with few exceptions (Kuntner etal. 2012), they cease
to grow at sexual maturity (Foelix 2011). In females, the
fecundity hypothesis is well corroborated (but see Higgins
etal. 2011). On the other hand, sexual selection by con-
test competition mostly favours larger males (Foellmer and
Fairbairn 2005; Kasumovic and Brooks 2011; but see Kralj-
Fišer and Kuntner 2012; Neumann and Schneider 2015),
but results regarding the relationship between male size and
success in sperm competition (Schneider and Elgar 2000;
Kralj-Fišer etal. 2013), mobility (Corcobado etal. 2010;
Quiñones-Lebrón etal. 2019), and sexual cannibalism (Elgar
etal. 2000; Kralj-Fišer etal. 2016) are mixed.
Heritability estimates of body size in sexually size dimor-
phic spiders vary between 0.14 and 0.48 (Uhl etal. 2004;
Turk etal. 2018), and studies report significant family effects
on life history traits (Neumann and Schneider 2016; Neu-
mann etal. 2017; Lissowsky etal. 2021). Spiders exhibit life
history plasticity in response to food availability (Uhl etal.
2004; Kleinteich and Schneider 2011), temperature (Li and
Jackson, 1996), photoperiod (Miyashita 1987; Schaefer 1977;
Lissowsky etal. 2021), seasonality (Higgins 2000; Lissowsky
etal. 2021), and social cues (Neumann and Schneider 2016;
Cory and Schneider 2018; Quiñones-Lebrón etal. 2021).
Sexes may differ in plasticity, but mixed evidence exists on
which sex is more plastic. For example, male Mediterranean
tarantulas (Lycosa tarantula) show greater plasticity in adult
size in response to food availability than females (Fernández-
Montraveta and Moya-Laraño 2007). In contrast, in cellar
spiders (Pholcus phalangioides), heritability of body size
ranges from 0.14 to 0.23 in females and 0.44 to 0.48 in males,
with females being the more plastic sex (Uhl etal. 2004). The
above studied spider species are relatively sexually monomor-
phic. Studies investigating life history trait plasticity in sexu-
ally size dimorphic representatives, however, remain scarce
(e.g. Neumann etal. 2017).
Here, we study life history traits in the sub-Saharan
African hermit spider, Nephilingis cruentata. Hermit spi-
ders exhibit extreme female-biased sexual size dimorphism
(eSSD sensu Kuntner and Coddington 2020), with a sexual
dimorphism index (SDI = mean female length/ mean male
length – 1) (Lovich and Gibbons 1992) averaging 3.22. In
addition to smaller body sizes affected by the developmental
response to food availability and social cues (though only in
well-fed spiders; see Quiñones-Lebrón etal. 2021), males
also exhibit at least two times shorter development times
(Kuntner 2007). Broad-sense heritability of male body size
was estimated at 17% (Quiñones-Lebrón etal. 2021).
Here we report on a long-term study that mated the fourth
laboratory-reared generation of spiders and reared their off-
spring in standardized laboratory conditions. Food availa-
bility, light regime, and temperature were standardized and

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comparable throughout the experiment, although we did
not control for natural daylight. Because natural daylight
can alter life history, e.g. the speed of development (e.g.
Lissowsky etal. 2021), we tested for a potential effect of
natural daylight on spider life histories by dividing the year
into three periods based on natural day length (see Methods)
and incorporated data on day length period at hatching into
the analyses.
We tracked individuals through their entire life and noted
their development time (i.e. time from egg hatching to matu-
ration), mass at maturation, total lifespan (time from egg
hatching to natural death), and adult longevity (time from
maturation to natural death). These experiments allowed us
to (i) assess intersexual differences in the four selected life
history traits, (ii) test if and how these traits correlate to each
other and if the recovered relationships suggest any trade-
offs between the traits, (iii) test which traits affect female
reproductive success, and finally, (iv) analyse what propor-
tion of total phenotypic variance in life histories and, in
females, fitness components are explained by family effects
and day length during development (fixed effect).
We predict high intrasexual variability in development
time, body mass at maturation, adult longevity, and total
lifespan. We expect that the spiders’ life history strategy
includes a trade-off between development time, body size at
maturity, and total lifespan and adult longevity, with shorter
development leading to maturation at smaller sizes and
longer adult lifespans. We expect heavier females to reach
greater reproductive success (e.g. Vollrath 1987; Uetz 1992).
Finally, as reproduction is costly and compromises survival,
we predict a shorter lifespan in mated compared to unmated
individuals (e.g. Chapman etal. 1998; Scharf etal. 2013).
Material andmethods
General rearing design
We used the extremely sexually size dimorphic African
hermit spider, Nephilingis cruentata (Fig.1), where body
length ranges 10–28mm in females and 3.1–3.9mm in
males (Kuntner 2007). The spiders came from the fourth
and fifth generation of a laboratory population, established
in 2015 at ZRC SAZU (Ljubljana, Slovenia). The seed popu-
lation of 40 females and 22 males was collected at iSiman-
galiso Wetland Park and Ndumo Game Reserve in KwaZulu-
Natal, South Africa (permit num. OP552/2015 by Ezemvelo
KZN Wildlife) in February 2015. In 2018, additional eight
females and one male were collected at iSimangaliso Wet-
land Park (permit number as above) and added to the labora-
tory population.
We reared spiders individually in transparent plastic cups
(250ml) with a cotton-filled hole to facilitate air and water
exchange. Twice a week, we sprayed them with water and
fed them by placing food items onto the webs they build in
the cups. The feeding regime was standardized. Males and
juvenile females until the fourth moult were fed Drosophila
sp. adlibitum, while larger juvenile and adult females were
fed twice per week with 1 and 3 blowflies (Lucilia sericata),
respectively. The temperature and light–dark regime in the
laboratory were constant (T = 25°C ± 2°C, LD 12:12h, but
see below).
To obtain offspring, we mated randomly chosen females
and males that were not siblings. A few days before each
mating, we placed the female in a methacrylate frame
(35 × 35 × 12cm), where she built a web. Using a paint-
brush, we gently transferred the male onto the female’s web
and left the pair together until they copulated, but at most for
4h, when they were separated. Nephilingis males generally
mate opportunistically — they approach females while they
are disturbed. To that end, we added blowflies onto the web
approximately 5min after adding the male. If they mated, we
noted the number of copulations and occurrence of sexual
cannibalism. We transferred the female back into her plas-
tic cup and checked for egg sacs at least twice a week. In
total, we mated 100 females and 75 males (25 males mated
with two different females) from both parental and offspring
generations. Of those, 87 females laid at least one viable egg
sac, which was left with the female until hatching.
The laboratory was lit with artificial lights at a constant
12-h day/12-h night regime, but we did not control for the
natural light seeping through windows. To test the effect of
day length on life history traits, we separated the year into
three periods: increasing day length (21st March to 20th
June), decreasing day length (21st June to 20th September),
and the period when the artificial day length in the labora-
tory was longer than natural day length (21st September to
Fig. 1 Female (large) and male (small) Nephilingis cruentata, an
extremely sexually size dimorphic spider

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20th March). We recorded the period during each egg sac
was hatched.
We transferred hatched spiders into a communal 200ml vial
with a foam cover and sprayed them twice a week. After 2weeks,
20 random spiders from each egg sac were put into individual
cups, where they were reared until adulthood as described above.
The remaining spiders from the clutch were discarded. In total,
we isolated 1740 hatchlings, of which 300 females and 655 males
survived to adulthood. Each spider was randomly assigned to
a specific treatment: they could either be mated (treatment 1;
N♀ = 119, N♂ = 84), left unmated (treatment 2; N♀ = 181,
N♂ = 305), or, for males only, left unmated and starved (treat-
ment 3; N♂ = 266). The latter were not included in analyses
including adult and total longevity and reproductive success but
were included in all other analyses. Starved males were later used
in experiments, unrelated to the present study.
We weighed the spiders using an electronic laboratory
scale (KERN GI 220–3 NM; min = 0.02, d = 0.00001g)
1day after maturation. We checked spiders five times a week
for moults and survival. Spiders were reared until their natu-
ral death and then preserved in 70% ethanol. We measured
the carapace width, a linear measure of body size, of all
preserved adult spiders using a stereomicroscope (Olympus
SZX9) and cellSens software (Olympus). To justify the use
of mass as a proxy of body size, we calculated Pearson’s
correlation coefficient between carapace width and mass at
maturation using R v. 3.5.3.
Traits assessed
In both the parental and offspring generations, we recorded
the date of hatching, date of maturation, mass at maturity,
and date of death. In mated females from the parental gen-
eration, we recorded the number of laid and hatched egg sacs
and the number and sex of offspring from the first clutch that
reached adulthood. If a male died of sexual cannibalism, we
did not include his data on total lifespan and adult longev-
ity into the analyses. We calculated the sexual dimorphism
index for body mass following Lovich and Gibbons (1992):
Statistical analyses
Prior to analyses, all recorded variables in each sex were
tested for normality using the Shapiro–Wilk test, included
in the R package stats (R Core Team 2019), to justify the
use of parametric statistical tests. We tested for differences
between the means of selected traits in the two sexes using
a two-sample t test, also included in stats. Next, to test the
effect of selected factors on the spiders’ life history traits, we
SDI
=
mean female weight
mean male weight
−
1
used two types of linear models. When relatedness among
individuals had to be controlled for through the random
effect family, we used mixed effects models, performed with
the package lme4 (Bates etal. 2015) in R v. 3.5.3. (R Core
Team 2019). We tested the statistical significance of each
tested fixed effect with ANOVA, comparing the full model
to its version without the tested fixed effect. We performed
the analyses on a subset of individuals with known data for
all effects, included in the model. When relatedness was not
relevant, we applied simple linear models from the package
stats. When body weights of both sexes were included in the
same model (in analyses related to egg sacs and offspring
survival), body weight data was log transformed due to the
large difference in scale between the masses of both sexes.
Results
Descriptive statistics
We report descriptive statistics for development time, mass
at maturity, total lifespan, and adult longevity in Table1.
For females, we also record the number of laid and hatched
egg sacs. Development time is considerably longer in
females than in males (females, 182 ± 35days, N = 294;
males, 79 ± 15days, N = 648). Females on average develop
2.3 times longer than males and are on average 75.2 times
heavier when reaching maturity (females, 0.4737 ± 0.1394g,
N = 295; males, 0.0063 ± 0.0021g, N = 648). The ranges of
both development time and mass at maturity are considerable.
Table.1 Descriptive statistics for development time, mass at maturity,
total lifespan, adult longevity, and, in females only, the number of laid
and hatched egg sacs. Males assigned to treatment 3 were omitted
from adult longevity and total lifespan calculations
Variable Mean SD Min Max N
Females
 Development time (days) 182 35 48 336 294
 Mass at maturity (g) 0.4737 0.1394 0.1773 0.9775 295
 Adult carapace width
(mm)
5.563 0.606 4.415 7.365 66
 Adult longevity (days) 179 103 2 406 240
 Total lifespan (days) 356 103 147 580 240
 Number of laid egg sacs 3 2 0 12 106
 Number of hatched egg
sacs
2207104
Males
 Development time (days) 79 15 42 134 648
 Mass at maturity (g) 0.0063 0.0021 0.0019 0.0181 648
 Adult carapace width
(mm)
1.358 0.14 1.055 1.915 481
 Adult longevity (days) 64 28 1 162 288
 Total lifespan (days) 143 29 64 263 288

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Females take 48 to 336days to mature, while their total lifes-
pan ranges between 147 and 580days and their adult longev-
ity (i.e. from maturation until death) from 2 to 406days. The
smallest female matured at only 0.1773g, which is 5.5 times
less than the largest, weighing 0.9775g at maturation. On
the other hand, developmental time in males ranged from
42 to 134days, adult longevity from 1 to 162days, and total
lifespan from 64 to 263days. The smallest male weighed
0.0019g and the largest 0.0181g, 9.8 times as much. Hence,
the average body mass sexual dimorphism index (SDI) in
our sample is 74.2, ranging from 8.8 (min female mass /
max male mass – 1) to 513.5 (max female mass / min male
mass – 1), while the average carapace width SDI is 3.1. The
Pearson’s correlation coefficient between carapace width and
mass at maturation is 0.8757 (p < 0.001) in males and 0.9054
(p < 0.001) in females. The differences in mean trait values
between sexes (Table1) are, expectedly, all highly statisti-
cally significant — development time, t (345.87) = 48.112,
p < 0.001; mass at maturity, t (294.06) = 57.504, p < 0.001;
adult longevity, t (268.27) = 16.813, p < 0.001; and total lifes-
pan, t (313.91) = 28.99, p < 0.001.
Development time
The first model tested the influence of day length (fixed
effect) on development time, with family as a random
effect. Day length significantly affects development time
in females (χ2 = 13.8, p = 0.001). Development time was
the shortest when daylight was increasing (March to June;
177.5 ± 3.6days, N = 184). In comparison, development time
was 31.7 ± 8.4days longer when day length was decreasing
(June to September, N = 40) and 9.1 ± 6.9days longer under
the constant laboratory light regime (September to March,
N = 76) (Table2). Family affiliation only explains 25.3% of
the total variance in development time, so residual random
variance, or within-family variance, is 74.7% (Table2).
Day length also significantly affects development time
in males (χ2 = 9.3, p = 0.009). Development time was the
shortest in increasing days (March to June, 78.2 ± 2days,
N = 425). In comparison, development time in decreas-
ing days was longer by 8.8 ± 3.9days (June to September,
N = 96) and longer by 10.7 ± 4.1days in days with constant
day length (September to March, N = 135) (Table2). With
59.6%, family affiliation explains more total variance in
development time than in females, leaving 40.4% remain-
ing within-family variance (Table2).
Body mass atmaturity
The second model tested how two fixed effects, devel-
opment time and day length, influence body mass at
maturity, with family as a random effect. Female mass at
maturity is significantly affected by day length at hatch-
ing (χ2 = 10, p = 0.007) and development time (χ2 = 46.5,
p < 0.001) (Fig.2a). Females hatched in decreasing days
(June to September) were 0.076 ± 0.029g heavier com-
pared to increasing days (March to June), while those from
days with constant day length (September to March) were
0.028 ± 0.023g lighter (Table3). Longer development
times lead to heavier females, with each additional day
of development adding 0.0015 ± 0.0002g (1.5 ± 0.2mg)
to adult body mass (Table3). Family relatedness explains
18.4% of total variance in female body mass at maturity
(Table3).
Male body mass at maturity is also significantly
affected by both day length at hatching (χ2 = 15.5,
p < 0.001) and development time (χ2 = 89.1, p < 0.001)
(Fig.2b). Males hatched in decreasing days (June to
September) were 1.163 ± 0.341mg heavier compared to
increasing days (March to June), while those from days
with constant day length (September to March) were
0.9939 ± 0.3247mg heavier (Table3). Each additional
day of development contributed 0.0501 ± 0.0051mg to
adult body mass (Table3). Family relatedness explains
25% of total variance in male body mass at maturity
(Table3).
Table.2 Results of linear mixed effect models with development time
as the dependent variable, day length at hatching as a fixed effect, and
family as a random effect in females (N observations = 291, N fam-
ily = 69) and males (N observations = 640, N family = 80). Significant
results (p < 0.05) are in bold
Predictors Development time (days)
Fixed effects Estimate SE t value
Females
 Intercept 177.521 3.576 49.639
 Day length 2 (decreas-
ing) 31.714 8.434 3.760
 Day length 3 (con-
stant) 9.111 6.909 1.319
 Random effects Variance SD % of total variance
 Family (intercept) 297 17.23 25.3
 Residual 876 29.60 74.7
Males
 Intercept 78.179 1.981 39.461
 Day length 2 (decreas-
ing) 8.751 3.944 2.219
 Day length 3 (con-
stant) 10.669 4.108 2.597
 Random effects Variance SD % of total variance
 Family (intercept) 185.1 13.61 59.6
 Residual 125.7 11.21 40.4

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Adult longevity
The third model tested for the effect of body mass at matu-
rity, day length, and development time (fixed effects) on
adult longevity, with family as a random effect. Female adult
longevity is significantly correlated only to treatment type,
i.e. mated or unmated (χ2 = 25.9, p < 0.001), where mated
females lived 66.4 ± 12.7days longer than unmated females
(Table4). Longevity is somewhat negatively affected by
development time and by decreasing and constant day
length at hatching, though not significantly (p = 0.067 and
p = 0.077, respectively) (Fig.3a). Adult body mass does not
show an effect on longevity (p = 0.199). Family explains
12.2% of total variance in female adult longevity (Table4).
Adult longevity in males depends on treatment type
(χ2 = 32.6, p < 0.001) and development time (χ2 = 12.8,
p < 0.001) but not on mass at maturity (p = 0.47) or day
length at hatching (p = 0.45). Mated males lived 23 ± 4days
longer than unmated males (Table4). Each additional day
of development shortened adult longevity for 0.4 ± 0.1days
(Table4; Fig.3b). Family explains 20.5% of total variance
in male adult longevity (Table4).
Total lifespan
The fourth model tested for the effect of body mass at
maturity, day length, and development time (fixed effects)
on total lifespan, with family as a random effect. In
females, total lifespan depends on day length (χ2 = 10.2,
Fig. 2 Relationship between
development time and adult
mass in a females and b males
Weight at maturity (gram)
Development time (day)
0.2
0.3
0.4
0.5
0.2
0.3
0.4
0.5
1.0
0.002
0.004
0.006
0.008
0.010
0.012
0.014
0.016
0.018
80 100 120 140 160 180 200 220 240 260 280 300 320
40 50 60 70 80 90 100 110 120 130
a
b

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p = 0.006) and treatment (χ2 = 20.3, p < 0.001) but not
on mass at maturity or development time (p = 0.98 and
p = 0.12, respectively). The lifespan of mated females was
58.8 ± 12.8days longer than of unmated females (Table5).
Females hatched in increasing days (March to June) lived
61.3 ± 22.9days longer than those hatched in decreasing
days (June to September) and 42.8 ± 18.2days longer than
those hatched during days with constant day length (Sep-
tember to March) (Table5). Family explains only 8.8% of
total variance in total female lifespan (Table5).
Total lifespan in males depends on development time
(χ2 = 22.8, p < 0.001) and treatment (χ2 = 32.6, p < 0.001).
The lifespan of mated males was 23.7 ± 4days longer than
of unmated males (Table5). Male total lifespan extended
for 0.6 ± 0.1days per each additional day of development
(Table5). Family explains 20.5% of total variance in total
male lifespan (Table5).
Number oflaid andhatched egg sacs
The fifth model tested for the effect of female (dams’) body
weight, male (sires’) body weight, their interaction, and
female (dams’) longevity on the number of laid and hatched
egg sacs. Both the number of laid egg sacs (F68,4 = 42.55,
p < 0.001) and hatched egg sacs (F68,4 = 14.13, p < 0.001)
depend on adult female longevity but not on female body
weight, male body weight, or their interaction. For each
additional day of life, females laid 0.02 ± 0.002 more
egg sacs — in other words, they laid one additional egg
sac for approximately every additional 50days of life
(p < 0.001) (Table6). Similarly, for each additional day
of life, 0.01 ± 0.002 egg sacs hatched — put differently,
one additional egg sac hatched for approximately every
additional 80days of a female’s life (p < 0.001) (Table6).
Offspring survival
The last, sixth, model tested for the effect of female (dams’)
body weight, male (sires’) body weight, and their inter-
action on offspring survival, i.e. the number of offspring
that reached maturity. The model (F78,3 = 1.117, p = 0.347)
did not find a significant effect of female body weight
Table.3 Results of linear mixed effects models with mass at maturity
as the dependent variable, day length at hatching and development
time as fixed effects, and family as a random effect in females (N
observations = 287, N family = 69) and males (N observations = 635,
N family = 80). Significant results (p < 0.05) are in bold
Predictors Mass at maturation (g)
Fixed effects Estimate SE t value
Females
 Intercept 0.1885 0.0398 4.737
 Day length 2
(decreasing) 0.0758 0.029 2.613
 Day length 3
(constant) − 0.0284 0.0231 − 1.229
 Development time 0.0015 0.0002 7.062
 Random effects Variance SD % of total variance
 Family (intercept) 0.0027 0.0521 18.4
 Residual 0.0121 0.11 81.6
Males
 Intercept 1.858e−03 4.216e−04 4.407
 Day length 2
(decreasing) 1.163e−03 3.41e−04 3.41
 Day length 3
(constant) 9.939e−04 3.247e−04 3.061
 Development time 0.501e−04 0.051e−04 9.874
 Random effects Variance SD % of total variance
 Family (intercept) 0.8563e−06 0.9253e−03 25
 Residual 2.567e−06 1.6020e−03 75
Table.4 Results of linear mixed effects models with adult longevity
as the dependent variable; mass at maturity, day length, development
time, and treatment (mated and unmated) as fixed effects; and family
as a random effect in females (N observations = 234, N family = 65)
and males (N observations = 284, N family = 75). Significant results
(p < 0.05) are in bold
Predictors Adult longevity (days)
Fixed effects Estimate SE t value
Females
 Intercept 269.9 37.5 7.194
 Treatment (unmated) − 66.4 12.7 − 5.232
 Day length 2 (decreas-
ing)
− 12.5 26.2 − 0.477
 Day length 3 (constant) − 41.9 18.6 − 2.252
 Body mass 66.5 53.2 1.250
 Development time − 0.4 0.2 − 1.805
 Random effects Variance SD % of total variance
 Family (intercept) 1151 33.93 12.2
 Residual 8280 91 87.8
Males
 Intercept 113 9.2 12.275
 Treatment (unmated) − 23 4 − 5.904
 Day length 2 (decreas-
ing)
5.7 5.6 1.002
 Day length 3 (constant) − 2.1 5.2 − 0.404
 Body mass 599.8 856.3 0.7
 Development time − 0.4 0.1 − 3.573
 Random effects Variance SD % of total variance
 Family (intercept) 139.6 11.81 20.5
 Residual 539.9 23.24 79.5

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_####_ Page 8 of 12
(p = 0.083), male body weight (p = 0.087), or their interac-
tion (p = 0.078) on offspring survival.
Discussion
Using a large sample, we characterize the following dif-
ferences between the sexes in Nephilingis cruentata.
Compared with males, females are on average 75.2 times
heavier and have a 3.2 times wider carapace, take 2.3 times
as long to reach sexual maturity, live 3.5 times longer as
adults, and have 2.5 times longer total lifespans. These
data suggest that females also have a higher growth rate
than males. Thus, N. cruentata spiders, which are among
the most sexually size dimorphic terrestrial inverte-
brate species (Kuntner and Coddington 2020), achieve
larger female sizes through faster and longer growth/
development.
Fig. 3 Relationship between
development time and adult lon-
gevity (time from maturity until
death) by treatment in a females
and b males
Adult longevity (day)
Development time (day)
0
40
80
120
160
200
240
280
320
80 100 120 140 160 180 200 220240 260280 300320
40 50 60 70 80 90 100110 120130
a
b
360
400
0
20
40
60
80
100
120
140
160
Mated Unmated

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We explain the detected high intrasexual variability in
life history traits by means of variability in family effects
(genetic plus maternal effects), environmental effects (day
length), and residual (uncontrolled) variance. Family effects
are strongest for development time (females 25%, males
60%), followed by mass at maturation (females 18%, males
25%), adult longevity (females 12%, males 20%), and total
lifespan (females 9%, males 20%). Following Moore etal.
(2019), family effects generally explain about 30% of vari-
ance in life history traits. Our estimates of family effects on
life histories in N. cruentata are mostly below 30%, which
is markedly lower compared to other studied spider species
(Uhl etal. 2004; Lissowsky etal. 2021). Interestingly, family
effects consistently have a greater effect on male compared
to female life histories, suggesting that the developmental
trajectories in males are more strongly channelled by genetic
factors and maternal effects. Given that males mature much
earlier than females, this difference may be mainly due
to maternal effects, which are expected to weaken during
ontogeny (Mousseau and Dingle 1991; Moore etal. 2019).
Considering that family effects on the traits studied are
small to moderate (with the exception of male development
time), life histories in these spiders seem to respond well
to environmental conditions. This is expected, as nephilid
spiders exhibit developmental plasticity in response to food
(Neumann etal. 2017; Quiñones-Lebrón etal. 2021), social
cues (Neumann etal. 2017; Quiñones-Lebrón etal. 2021),
and seasonality (Higgins 2000; Lissowsky etal. 2021). Here,
we controlled for environmental conditions (food, tempera-
ture, direct social cues, humidity, laboratory light regime),
except for natural light seeping through windows. As in
some other spider species (Schaefer 1977; Miyashita 1987;
Lissowsky etal. 2021), N. cruentata spiders also respond to
light conditions during development. Development time is
shortest in spiders hatched during increasing daylight and
significantly longer in spiders hatched during decreasing
daylight in both sexes.
In addition, we test for potential trade-offs between life
histories, as well as sex differences in these trade-offs. As
expected, we find a negative correlation between develop-
ment time and mass at maturity in both sexes. Following the
trade-off between development time and size at maturation,
spiders hatched during increasing day length matured at a
lower body mass than those hatched during decreasing day
length. Such a response to photoperiod was also observed
in a natural population of the nephilid species Trichone-
phila clavipes, where day length relates to the start of an
individual’s reproductive period or the end of the season
(Higgins 2000).
In spiders, the relationship between male size and mat-
ing success generally largely depends on competition sce-
narios (Kasumovic and Andrade 2009; reviewed in Andrade
2019). When competition between males is low, the optimal
Table.5 Results of linear mixed effects models with total lifespan as
the dependent variable; mass at maturity, day length, development
time, and treatment (mated and unmated) as fixed effects; and family
as a random effect in females (N observations = 270, N family = 68)
and males (N observations = 284, N family = 75). Significant results
(p < 0.05) are in bold
Predictors Total lifespan (days)
Fixed effects Estimate SE t value
Females
 Intercept 334.7 36.1 9.277
 Treatment (unmated) − 58.8 12.8 − 4.6
 Day length 2 (decreas-
ing) − 61.3 22.9 − 2.68
 Day length 3 (constant) − 42.8 18.2 − 2.357
 Development time 0.3 0.2 1.534
 Body mass 1.4 52.7 0.027
 Random effects Variance SD % of total variance
 Family (intercept) 948.6 30.80 8.8
 Residual 9789.7 98.94 91.2
Males
 Intercept 112.5 9.2 12.275
 Treatment (unmated) − 23.7 4 − 5.904
 Day length 2 (decreas-
ing)
5.7 5.6 1.002
 Day length 3 (constant) − 2.1 5.2 − 0.404
 Development time 0.6 0.1 4.848
 Body mass 599.8 856.3 0.7
 Random effects Variance SD % of total variance
 Family (intercept) 139.6 11.81 20.5
 Residual 539.9 23.24 79.5
Table.6 Results of linear models, estimating the effect of female
mass, male mass, their interaction, and female longevity on the num-
ber of laid (N obser vations = 88, total N egg sacs = 339) and hatched
egg sacs (N observations = 88, total N egg sacs = 256). Significant
results (p < 0.05) are in bold
Predictors
Fixed effects Estimate SE t value
Laid egg sacs (number)
 Intercept 4.96 7.96 0.623
 Adult longevity 0.02 0.002 12.147
 Female mass (log) 0.39 8.05 0.049
 Male mass (log) 1.34 1.55 0.861
 Interaction F mass:M mass 0.56 1.56 0.361
Hatched egg sacs (number)
 Intercept − 3.77 8.69 − 0.434
 Adult longevity 0.01 0.002 6.781
 Female mass (log) − 5.45 8.79 − 0.62
 Male mass (log) − 0.57 1.7 − 0.338
 Interaction F mass:M mass − 0.72 1.7 − 0.424

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_####_ Page 10 of 12
growth pattern shifts to maturation at the minimum size that
sustains gonadal investment and success in the scramble for
mates (Quiñones-Lebrón etal. 2021). However, males of N.
cruentata eventually aggregate around females and guard
them after copulation (Kuntner 2007), so they are in direct
competition, and large size might generally be preferred
(Kasumovic and Brooks 2011; but see Kralj-Fišer and Kunt-
ner 2012). Our data suggest that males mature earlier and
at smaller sizes early in the reproductive season and mature
at larger sizes later in the reproductive season when they
might be more likely to encounter rival males. It is possible
that males use different environmental cues to adjust their
maturation timing, including day length. Indeed, we found
that males that develop in increasing daylight have shorter
development times then those developing during decreasing
daylight. Thus, we hypothesize male size to be under oppos-
ing selection forces, and developmental plasticity may allow
for adjustments in developmental trajectories to account for
expected competition (Andrade 2019). Namely, males with
longer developmental times grow to larger sizes but have a
shorter adult lifespan. Thus, males follow the expected life
history path in which prolonged development shortens their
adult longevity and balances their total lifespan (see above).
Similarly, females that mature earlier are smaller than
those with longer development. In theory, in seasonal cli-
mates, early-maturing smaller females pay the cost of low
fecundity but have more time for reproduction, while, con-
versely, late-maturing females are larger and more fecund
but may be subjected to an end-of-season penalty, e.g. lim-
ited mating opportunities and a short reproductive period
(Stearns 1992; Higgins 2000). Our results partly meet these
theoretical expectations. Namely, female mass does not cor-
relate to reproductive success, refuting the overall validity of
the fecundity hypothesis (Head 1995). However, we found a
negative correlation between female development time and
adult longevity. Adult longevity further influences female
reproductive success: females produce egg sacs in rather
consistent intervals throughout their adult life, and the num-
ber of egg sacs is therefore related to longevity rather than
female mass. In other words, females that develop for a long
time mature at a larger body mass but live for a shorter time
and produce fewer egg sacs and vice versa. Future studies
should apply more precise fecundity measures, e.g. the num-
ber and size of eggs.
In both males and females, adult longevity and total lifes-
pan depends on the mating status. Namely, the spiders that
copulated live longer than those left unmated. These results
are in disagreement with other studies (Chapman etal. 1998;
Scharf etal. 2013). Although puzzling, our finding could be
explained by the mating system in N. cruentata. As in sev-
eral nephilid species, males of N. cruentata have a mono-/
bigamous mating system, as they lose their sperm-transfer-
ring organs (pedipalps) during copulation. Sterile eunuch
males then remain with females and guard them against
rival males. In another nephilid, Nephilengys malabaren-
sis (Walckenaer, 1841), eunuch males have an advantage
in direct male–male contests (Kralj-Fišer etal. 2011) and
show enhanced stamina (Lee etal. 2012). Eunuch males
might benefit from lower energy costs, i.e. having lighter
bodies (Lee etal. 2012) and access to prey in the female’s
web, which may explain their longer lifespans. Similarly,
increased female longevity in mated females after matu-
ration is puzzling. We suggest two possible explanations:
(1) hormonal changes that prolong adult longevity and (2)
costs related to carrying unfertilized eggs. Although female
spiders generally lay unfertilized eggs if unmated, we have
never observed such behaviour in N. cruentata, hinting at
the possibility of such fitness costs.
There is a growing interest in the study of develop-
mental plasticity in spiders and its relationship with life
history traits and the evolution of sexual size dimorphism
(Andrade 2019). Sexual divergence in developmental tra-
jectories of sexually dimorphic spiders seems to be the
norm and may reflect early differences in the processes
underlying growth (Cordellier etal. 2020). We provide
evidence for sex differences in the contribution of genet-
ics and maternal effects (i.e. family effect) on each of the
measured life history traits. We additionally provide evi-
dence for differences in life history trade-offs that corre-
spond to sex-specific selection pressures.
Author contribution Conceptualization, ideas and formulation or
evolution of overarching research goals and aims: Simona Kralj-Fišer
(SKF).
Field work and specimen acquisition: Matjaž Kuntner (MK),
Charles R. Haddad (CRH), Matjaž Gregorič (MG), Tjaša Lokovšek
(TL), Klemen Čandek (KČ), and Shakira Quinones (SQ).
Animal rearing: lead, Rok Golobinek (RG); equal, TL, Eva Turk
(ET), Janko Šet (JŠ), and SKF; support, MG and SQ.
Data curation, management activities to annotate (produce meta-
data), scrub data, and maintain research data (including software code,
where it is necessary for interpreting the data itself) for initial use and
later re-use: RG, JŠ, TL, and SKF.
Formal analysis, application of statistical, mathematical, computa-
tional, or other formal techniques to analyse or synthesize study data:
ET.
Funding acquisition, acquisition of the financial support for the
project leading to this publication: SKF and MK.
Investigation, conducting a research and investigation process, spe-
cifically performing the experiments, or data/evidence collection: lead,
SKF; equal, RG, ET, JŠ, and TL.
Methodology, development or design of methodology, and creation
of models: SKF and ET.
Project administration, management, and coordination responsibil-
ity for the research activity planning and execution: SKF.
Supervision, oversight and leadership responsibility for the research
activity planning and execution, including mentorship external to the
core team: SKF.
Validation, verification, whether as a part of the activity or separate,
of the overall replication/reproducibility of results/experiments and
other research outputs: SKF.

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Page 11 of 12 _####_
Visualization, preparation, creation, and/or presentation of the pub-
lished work, specifically visualization/data presentation: ET (graphs,
tables) and MG (photo).
Writing — original draft, preparation, creation, and/or presentation
of the published work, specifically writing the initial draft (including
substantive translation): SKF, ET, and JŠ.
Writing — review and editing: JŠ, ET, RG, TL, MG, SQ, CRH,
KČ, MK, and SKF.
Preparation, creation, and/or presentation of the published work
by those from the original research group, specifically critical review,
commentary, or revision, including pre- or post-publication stages:
SKF.
Revision: ET and SKF.
Funding The authors were supported by the Slovenian Research
Agency (grants P1-0236, P1-0255, J1-9163).
Data availability Data will be available on Dryad after acceptance.
Declarations
Ethics approval Research on spiders is not restricted by the animal
welfare law of the country where the study was conducted. In the field,
we collected the minimum number of individuals needed to conduct the
research. The spiders were kept in conditions similar to their natural
environmental conditions. The spiders were regularly fed with differ-
ent prey items. The study was non-invasive. After the experiments, the
spiders remained in the laboratory and were reared until natural death,
as described above.
Consent for publication The manuscript was read and approved for
submission by all authors.
Conflict of interest The authors declare no competing interests.
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