Abstract
Sexual size dimorphism (SSD) arises when natural selection and sexual
selection act differently on males and females. Rensch’s rule predicts
that SSD increases with body size in species when males are the larger
sex. However, male-biased SSD is rare in insects and the rule does not
always hold between species and even among populations. Here, we
investigate intra-specific variation in SSD as well as relative
investment in precopulatory (horn length) and postcopulatory traits
(sperm length and testes weight), in a tropical rainforest dung beetleOnthophagus babirussa across Singapore and Peninsular
Malaysia. Overall, three out of four populations displayed significant
male-biased SSD but contrary to Rensch’s rule, SSD was greater in
populations with smaller overall body size. Average male body size was
similar across all populations, but female body size differed
significantly suggesting that the pronounced SSD may also be due to
weaker fecundity selection on female body size. Across all populations,
horn length showed a strong positive static allometry while
postcopulatory traits showed negative allometry (in all but one
population), which suggests an evolutionary trade-off between
precopulatory and postcopulatory traits in this species. (183 words)
Keywords : Sexual size dimorphism, Dung beetle, Southeast Asia,
Rensch’s rule, Reproductive evolution, Sexual selection
Introduction
Sexual selection is defined as selection on heritable traits that vary
between individuals within a population that influence reproductive
success and fitness (Andersson, 1994). When individuals within a
population have differential reproductive success (Panhuis et al.,
2001), this can occur prior to copulation (precopulation), when males
compete for access to females, leading to evolution of sexual dimorphism
in size and secondary sexual traits such as ornaments and weapons
(Simmons & García-González, 2008). Sexual selection can also occur
postcopulation, for example in the form of cryptic female choice, where
females can influence the success rate of insemination by males and/or
via sperm competition, where sperm from different males compete to
fertilise the ova (Birkhead & Pizzari, 2002).
One of the most common traits that is subject to sexual selection is
body size. Sexual size dimorphism (SSD) arises when the effects of
natural selection and sexual selection act differently on males and
females (Blanckenhorn, 2005). In fact, across species, when males are
larger, SSD is predicted to increase with overall body size, but
decreases with size when females are larger (sensu Rensch’s rule)
(Rensch, 1959). This phenomenon has been well documented across numerous
taxa especially vertebrates (Fairbairn 1997; Dale et al. 2007; Székely
et al. 2004). However, in most invertebrates, such as insects, species
often display female-biased SSD, where females are larger due to strong
fecundity selection. Larger male body size is usually a derived trait in
most insect lineages and numerous species present exceptions to the rule
(Blanckenhorn et al 2004; Blanckenhorn, Meier & Teder, 2007). For
instance, SSD can even vary significantly within a species but not many
studies address population differences in SSD (Teder & Tammaru, 2005;
Cox & Calsbeek, 2010; Puniamoorthy et al. 2012; Liao, Liu & Merilä,
2015; Piross et al 2019; Rossi and Haga 2019).
Species belonging to the dung beetle genus, OnthophagusLatreille, 1802, the most species rich genus in the animal kingdom, have
been gaining increased interests as models in sexual selection research
because many species display strong sexual dimorphisms (Parzer &
Moczek, 2008). Males often possess horns, a precopulatory sexual trait,
on the head and/or thorax which are used in defending breeding tunnels
occupied by females (Garcia-Gonzalez & Simmons, 2011; Kijimoto et al.,
2009; Simmons & García-González, 2008). For instance, in certainOnthophagus species, male horn lengths might trade-off with male
investment in testes and sperm and even maternal effects, such as larval
food provisioning, could affect variation in these male phenotypes
(Emlen, 1994; Emlen, 1997a; Moczek, 1998; Silva et al., 2016). These
studies often include work on O. taurus (Schreber, 1759), native
to the Mediterranean and exotic ranges in Eastern and western North
America and Australia, and O. acuminatus Harold, 1880, native to
Central America (Emlen, 1994; Emlen, 1997a; Moczek, 1998; Silva et al.,
2016). However, there is relatively little information on
population-level differences in reproductive trait variation in
Southeast Asian Onthophagus species (Parrett & Knell, 2018;
Parrett et al., 2019; Parrett et al., 2021). Previous reports on AsianOnthophagus species do not report male-biased SSD among species
(Goh & Hashim, 2020; Pomfret & Knell, 2006) but preliminary surveys in
Singapore indicated that there were some species where wild-caught males
were consistently larger than females. Here, we study variation in SSD
in one such species: Onthophagus babirussa (Coleoptera:
Scarabaeidae; Eschscholtz, 1822) which is a widespread species across
SEA (Goh, 2014; Kudavidanage, Qie, & Lee, 2012; Priawandiputra et
al. , 2020; Toh, 2019). Specifically, we investigate variation in both
precopulatory and postcopulatory traits within and between four
different populations from Singapore and Peninsula Malaysia.
We used DNA barcoding to confirm the genetic distinction of O .babirussa from morphologically similar species such as O .rufiobscurior Ochi, Kon and Tsubaki, 2009 and assess genetic
variation across all sampling sites. We tested if SSD varies among
populations and if this difference between the sexes increased with body
size (sensu Rench’s rule). In addition, we investigated male
investment in a precopulatory trait (horn length) and postcopulatory
traits (testes weight and sperm length) by calculating static allometry,
a widely used tool in quantifying relative investment in traits as a
function of body size (Eberhard et al. , 2018). Prior studies
suggest that there may be potential trade-offs in the investment of
precopulatory and postcopulatory traits given the limited resources for
development (Moczek & Nijhout, 2004). As beetle horns are important in
mate acquisition (Simmons & Ridsdill-Smith, 2011), we tested the
hypothesis that there would be a high investment in beetle horns, hence
a positive allometry and that the allometric coefficient for
postcopulatory traits would be lower than that of horns.