The evolution of male and female reproductive traits in simultaneously hermaphroditic terrestrial gastropods

Our understanding of postcopulatory sexual selection forcing reproductive trait evolution
continues to be illuminated by comparative studies. Inter- as well as intraspecific
comparisons offer the opportunity to study the long-lasting processes of diversification and
allow testing for correlated evolution between different traits. Moreover, morphological
studies provide important insights into the function and adaptive significance of specialised
reproductive organs.
In this thesis, I combined comparative studies on the inter- and intraspecific
evolution of female sperm storage organs (spermathecae) and sperm traits in
stylommatophoran gastropods with detailed studies on the influence of spermatheca
morphology on sperm storage patterns and the adaptive function of the bursa tract
diverticulum, an organ of the reproductive tract of snails associated with sperm digestion,
in the helicid land snail Arianta arbustorum.
In order to assess the pattern of sperm storage organ divergence across 47 species
of stylommatophoran snails and slugs partial 28S rDNA sequences were used to construct
a molecular phylogeny. Maximum likelihood as well as Bayesian methods were applied to
investigate the history of spermatheca origination and to test different hypotheses of
spermatheca evolution. The results revealed a large variation in the presence/absence of a
spermatheca and its structural complexity across stylommatophoran gastropods. The
evolution of spermathecae in the carrefour appeared to be associated with the evolution of
other peculiar morphological traits of the reproductive tract, e.g. love-dart shooting, as well
as with flagellum and diverticulum length. Moreover, a close relationship of spermatheca
presence with cross-fertilization as the predominant mating system was found. In addition,
the presence of complex spermathecae was coupled with several life-history traits,
including body size, reproductive strategy (semelparity vs. iteroparity) and reproductive
mode (oviparity vs. ovoviviparity), and with habitat specificity. Sperm length, highly
diverse in this species group, appeared to be adapted to the length of the sperm storage
organ. The results suggest an important influence of postcopulatory sexual selection on
spermatheca divergence. However, also life-history traits and habitat specificity might
have shaped the pattern of spermatheca distribution found across stylommatophoran
gastropods.
A closer look at male and female reproductive trait divergence, focussing on sperm
traits and sperm storage organ size, was taken using six natural populations of Arianta
arbustorum. The intraspecific variation in spermatophore volume, number of sperm
transferred and sperm length as well as in volume and length of the spermatheca and the
number of sperm storage tubules was quantified and the covariation between interacting
traits was examined. A significant among-population variation was revealed for all traits
except for spermatheca length. Furthermore, a positive association was found between the
number of sperm transferred and spermatheca volume. In accordance with the interspecific
study, these results indicate a strong influence of antagonistic coevolution on male and
female reproductive trait evolution.
Beside size and morphology of sperm storage organs, the physical properties of the
spermatheca may be important for the potential to exert cryptic female choice. This was
investigated by examining structure, volume and tubule length of empty spermathecae of
A. arbustorum and assessing differences in spermatheca size following a single copulation.
The study revealed that spermathecae of this species are expandable and can accommodate
more sperm than would be expected from measuring its initial volume. Moreover, neither
the volume of sperm stored in the spermatheca nor the amount of allosperm digested in the
bursa copulatrix were related to the size of the spermatophore received. These findings
suggest that the female function may be able to control sperm storage and sperm use.
Finally, the morphology and function of the bursa tract diverticulum, which serves
as a place of spermatophore uptake when present, was studied. Using histological,
histochemical and morphometrical methods it could be shown that the diverticulum is
involved in the digestion or at least in the partly breakdown of received spermatophores.
Furthermore, the positive allometry and the high phenotypic variation of diverticulum
length compared to shell size suggest directional sexual selection on this trait. Combining
evidence from this and previous studies indicates that the diverticulum is involved in the
coevolution of the complex reproductive traits of stylommatophoran gastropods.