All dysderid spiders studied adopt the same copulatory posture of H. sadistica
(e.g. Jackson & Pollard 1982
; Gerhardt 1933
), but in no other species is it known for males to pierce the female's body with their cheliceral fangs during courtship or to inject sperm by piercing the female's body wall. Furthermore, the genitalia of both the male and the female of H. sadistica
are modified in ways that are compatible with TI. The other species of the genus Harpactea
usually possess emboli which lack a terminal point (e.g. Chatzaki & Arnedo 2006
). The needle-like structure of the male's embolus functions in penetrating the female body wall, and the organs that females of other dysderid species would use for sperm acceptance and storage have atrophied in the female of H. sadistica
. Apparently TI is obligate in this species. Other spiders fertilize eggs in the uterus by moving sperm from spermathecae shortly before oviposition (Foelix 1982
), but H. sadistica
eggs are fertilized in the ovaries (internal fertilization) and the female lays embryos instead of single-cell eggs. The eggs of spiders bulge out from the ovaries into the body cavity (Foelix 1982
), and this might facilitate the finding and fertilizing of the eggs by spermatozoa travelling through the female's body cavity.
Females of dysderid spiders have cul-de-sac spermathecae (i.e. a single duct serves as both inlet and outlet for sperm) and the expectation for species with cul-de-sac spermathecae is that the last male to inseminate the female will tend to have his sperm used first to fertilize the eggs (Austad 1984
). Moreover, when females have cul-de-sac spermathecae, the sperm from males that mate with the female first are vulnerable to removal by males that mate later (Huber & Eberhard 1997
). Among dysderid species, it is common for females to mate readily with different males (M. Řezáč 2007, unpublished data), an inevitable consequence of this being strong competition among males for paternity. By practising TI, H. sadistica
males seem to have reversed the last-male sperm priority pattern, i.e. for H. sadistica
, the sperm from the first male to mate via TI should reach the eggs first (b
) and are protected from removal. There are three mutually exclusive hypotheses that might potentially explain the evolution of TI:
A schematic of two types of female genitalia with hypothetical sperm route. (a) ‘Cul-de-sac’ type representing all dysderid spiders (including Harpactea) with ‘normal’ insemination. (b) Atrophied type in H. sadistica.
. Sexual selection, particularly sperm competition (sensu Parker 1970
), underlies the evolution of TI, which might have evolved as an adaptive strategy by which first males circumvent an unfavourable structure of the female's sperm-storage organs. In other words, the males partly wrest control of fertilization from females. Nevertheless, intersexual conflict of interests should not be considered responsible for the evolution of this male trait as the primary selective force is the competition for paternity, while subduing female interests is its consequence. This hypothesis could be tested by studying the pattern of paternity in H. sadistica
and in its close relatives. It predicts that in H. sadistica
first males will be fathers of higher percentage of offspring than in relatives practising the conventional mode of fertilization. The sperm competition hypothesis may also help explain the evolution of TI in other groups of arthropods (Cimicomorpha, Strepsiptera, Malacosoma
), as the out-group of each of these also has cul-de-sac spermathecae (Snodgrass 1935
Hypothesis 2. TI could have evolved under natural selection. Internal fertilization leading to vivipary could be advantageous if juveniles laid as embryos possess higher survivorship than juveniles laid as eggs. But the female might secure internal fertilization more easily than via TI. This hypothesis could be tested by studying the survivorship of juveniles of H. sadistica and juveniles of its close relatives. It predicts that juveniles of H. sadistica will exhibit higher survivorship than juveniles of oviparous relatives.
Hypothesis 3. TI might also have evolved through female selection for good genes. For polyandrous females, it might be advantageous to create an inhospitable environment that allows only the most vigorous sperm to fertilize their eggs. In such a race among females to create the most difficult arena for sperm competition, they could have reduced the genitalia and sperm storage organs. TI could have been the male solution for where to deposit the sperm. The same process could be explained by intersexual conflict over control of mating and fertilization which, however, rests on specific assumptions, that are poorly known. This hypothesis could be tested by comparative study of female genitalia in the genus Harpactea. It predicts that there is tendency to reduce female genitalia in this genus.
The following paragraphs further elaborate the hypothesis 1 based on sperm competition. The evolution of TI may have started in species where sperm occasionally escaped from the female's genital tract and travelled through the haemocoel to her ovaries, as is known to happen in some mite species (Alberti 2002
). Further evolutionary steps could be represented by species where the males regularly injure the female genital organ during copulation in order to help sperm to escape and where males directly inject sperm into the coelom through the inner wall of the female's genitalia (intra-genitalic TI), as is known for Drosophila
). This requires sperm mobility and the female immune system to co-evolve for sperm to reach the eggs by moving through the female's haemocoel. These adaptations might, in turn, have added to the advantage for the male in shortcutting the route and injecting sperm outside the female genitalic region, closer to the ovaries. Hence, in groups which have acquired adaptations related to hemocoelic insemination, the evolution of extra-genitalic TI might be expected. In particular, this hypothesis might explain the multiple independent emergence of extra-genitalic TI in the heteropteran group Cimicomorpha (Tatarnic et al. 2006
Injuries inflicted by males through TI might incur a significant cost to females through physical damage and the risk of infection (see Reinhardt et al. 2005
). Therefore, one would expect that females would have evolved some defensive adaptations. Such adaptations were not found. Avoiding males that practise TI would be disadvantageous, as sons of females mated with males bearing the TI trait should themselves be more successful in circumventing the structure of the female spermathecae and thus obtaining fertilizations (in accordance with the theory of sexy sons). If the health costs outweighed the profit from good genes, females would probably eliminate this male strategy. Possible protecting adaptations (e.g. integument preventing haemolymph loss) would also be advantageous for the male because they protect his offspring. Females of other arthropods appear to have mitigated TI-derived costs by evolving secondary genitalic structures (Siva-Jothy 2006
). In some Drosophila
species, secondary spermathecae evolved in places where males of related species damage the genitalic wall (Kamimura 2007
). In the Cimicidae secondary sperm induction pores and secondary ducts leading to primary genitalia have evolved (Carayon 1966
). Similar secondary structures occur in butterflies (ditrysian genitalia; Grimaldi & Engel 2005
) and in spiders (secondary spermathecae or entelegyne genitalia, both of which have evolved independently several times; Brignoli 1978
; Forster 1980
). The evolution of these features has been heretofore difficult to explain. Yet it is of interest that, in both spiders and butterflies, there appears to be preadaptation of sperm to travel through the female's haemocoel en route
to fertilizing her eggs. Perhaps the secondary genitalic structures of butterflies and spiders could have originated via TI as well. Instead of being merely a zoological curiosity, TI may be more common among arthropods than previously thought and it may have been an important driving force in evolution of arthropod genitalia.