4. Discussion
4.1. Sexual size
dimorphism (SSD) varied among populations
According to the differential equilibrium model, SSD arises from the
equilibrium of three major evolutionary forces that acts differently on
body size – sexual selection that selects for larger body size in
males, fecundity selection that selects for larger body size in females
and viability selection (e.g. natural selection) that select against
large body size in both sexes, within general constraints (e.g. genetic,
physiological etc.) (Blanckenhorn, 2005). In addition, Rensch’s rule
predicts that in species that exhibit male-biased SSD, the differences
between the sexes increases with average body size and this is a
well-supported phenomenon in vertebrates (Rensch, 1959).
Unlike birds and mammals, most insects exhibit female-biased SSD, where
females have a larger body size (Blanckenhorn, 2005; Esperk et
al. , 2007; Rudoy & Ribera, 2017; Stillwell et al. , 2010). In
beetles, only 9% of the reported species exhibit male-biased SSD while
72% exhibit female-biased SSD (Stillwell et al. , 2010). However,
more specifically among the Onthophagus species, most do not
display sexual size dimorphism (Pomfret & Knell, 2006). In fact, a
study of six Southeast Asian Onthophagus species, includingO. Babirussa (from Peninsula Malaysia), reported no sexual
size dimorphism (Goh & Hashim, 2020). In our study, we documented
significant male-biased SSD in both Singapore populations (CCNR and
Pulau Ubin) and Langkawi (Figure 8 and appendix 4). Populations from
Peninsula Malaysia had larger males but the difference between the sexes
was not significant, thus replicating the results reported in Goh &
Hashim (2020).
Theory suggests that strong precopulatory sexual selection drives
male-biased SSD in insects as larger body size in males have been widely
documented to increase mating success due to female choice or male-male
competition (Blanckenhorn, 2005; Puniamoorthy, Schäfer, & Blanckenhorn,
2012; Stillwell et al. , 2010). In many Onthophagus dung
beetles and related taxa, males compete to gain access to females and
body size is a predominant factor in determining fighting success
(Emlen, 1997; Moczek & Emlen, 1999). However, the intensity of sexual
acting male body size is not necessarily stronger than the fecundity
selection acting on female body size. In beetles, larger females are
generally able to produce larger and more offspring, thus accounting for
the female-biased SSD observed in most species (Stillwell et al. ,
2010). As such, the male-biased SSD in O. barbirussa is likely a derived
trait that can be due to a relative increase in the intensity of sexual
selection on male body size in this species.
Based on the Rensch’s rule, one may predict that the SDI index or the
difference between the sexes is most pronounced in the populations where
body size is the largest i.e. the Malaysia populations. Instead, we
document that SSD is most pronounced in the Singapore populations (CCNR
and Pulau Ubin) where overall body size is the smaller. This is unlikely
due to stronger sexual selection on males as the body size of males did
not differ significantly between males of Singapore and Malaysia
populations. Rather, larger SSD in Singapore was more likely due to
weaker fecundity selection and/or stronger viability selection on
females in Singapore as females were significantly smaller in Singapore
than in Malaysian populations.
In Singapore, approximately 95% of forests were cleared over the last
200 years due to urbanisation, causing high local extinctions of fauna
such as birds and mammals in forest habitats (Bickford et al. ,
2010; Brook, Sodhl, & Ng, 2003). Singapore’s remaining forests are
mostly degraded, highly fragmented and often subjected to high levels of
disturbances, leading to a decrease in the general abundance of mammals
(Bickford et al. , 2010; Lee et al. , 2009). Thus, there are
fewer food and brood resources, leading to lesser opportunities for
oviposition in female dung beetles in Singapore where the main sources
of dung are likely from long-tailed macaques (Macaca
fascicularis ) and wild boars (Sus scrofa ) (Culot et al. ,
2013). In contrast, the sites surveyed in Malaysia is located within
larger stretches of forests that serve as a refuge for larger mammals
not found in Singapore, such as Asian elephant (Elephas maximus )
and Malayan Tapir (Tapirus indicus ), that are likely able to
provide more food and brood resources for oviposition opportunities for
female (Qie et al. , 2011; Rufino et al. , 2010). Hence,
lesser food resources in Singapore suggests that there could be a
stronger viability selection on females in Singapore compared to
Malaysia, leading to smaller female body size and male-biased SSD in
Singapore populations. In addition, there could also be weaker fecundity
selection on Singapore females because of lesser brood resources.
4.2 Investment in
precopulatory and postcopulatory traits varied among populations
Sexual selection can occur before copulation, where males invest in
precopulatory traits to increase mating opportunities and after
copulation, where males invest in postcopulatory traits to increase
chances of fertilising the ova of females (Birkhead & Pizzari, 2002;
Eberhard et al. , 2018). Our results show that all four
populations showed strong positive static allometry for horn length
where horns are disproportionately longer in larger individuals. In dung
beetles, horns are weapons used in male-male combat to gain access to
breeding females, strong precopulatory sexual selection on horns could
explain the strong positive static allometry in male O. babirussa(Emlen, Lavine, & Ewen-Campen, 2007; Simmons & Ridsdill-Smith, 2011).
Furthermore, compared to the allometric coefficient of classic case
studies of sexually selected traits such as deer antlers (β=1.86) and
rhinoceros beetle horns (β=4.15), the allometric coefficient for maleO. babirussa horns was approximately twofold (Figure 9a, β =8.552
– 9.685), further suggesting the presence of strong precopulatory
sexual selection on horns (Kodric-Brown, Sibly & Brown, 2006).
Despite the importance of possessing larger horns in gaining access to
females, males with small body sizes and small horns were still
regularly sampled and seem to persist in wild populations (Figure 4a).
In many Onthophagus species, males with small horns utilise
alternative mating strategies in which they masquerade as females to
sneak past guarding males with larger horns to gain access to breeding
females (Simmons & Ridsdill-Smith, 2011). Perhaps such an alternative
mating strategy exists in O. babirussa , which could explain the
phenotypic variation in horn length observed in wild-caught populations
(Moczek & Emlen, 2000).
Due to limited resources for growth and development, there may
potentially be trade-offs in the investment of precopulatory and
postcopulatory traits (Moczek & Nijhout, 2004). As there was a high
relative investment in horn length, a precopulatory trait, we
hypothesized that there would be a low relative investment in
postcopulatory traits such as testes weight and sperm length. We would
also then expect a lower allometric coefficient compared to horn length
allometry. As predicted, our results show a negative allometric
relationship for sperm length (β<1) for all populations,
suggesting that there is a lower relative investment in sperm length
than horns which could be due to weaker postcopulatory selection in maleO. babirussa. To test this, further studies would be
needed to identify the rates of polyandry in wild-caught O.babirussa populations by determining paternity estimates of
offspring to determine the intensity of postcopulatory sexual selection
via sperm competition (McCullough, Buzatto, & Simmons, 2017).
Interestingly, a positive allometric relationship for testes weight (β=
2.977) was found in Central Peninsula MY while the rest of the
populations had a negative allometric relationship with testes weight
(β<1). Males from Central Peninsula MY have similar body sizes
to those from Langkawi and Singapore, but with larger testes. This
suggests that there is a higher relative investment in postcopulatory
traits in Central Peninsula MY. This could be due to stronger
postcopulatory selection arising from sperm competition, as many studies
have shown that species under stronger selection often have larger
testes (Simmons & García-González, 2008). To test this, further studies
would be needed to assess the level of sperm competition between males
to determine if males in Central Peninsula MY have a competitive
fertilisation advantage compared to the rest of the populations (Simmons
& García-González, 2008).