Behavioral Ecology
doi:10.1093/beheco/arr053
Advance Access publication 1 June 2011
Forum: Ideas
Sperm dynamics in spiders
M.E. Herberstein,a J.M. Schneider,b G. Uhl,c and P. Michalikc
Department of Biological Sciences, Macquarie University, North Ryde, NSW 2109, Australia, bZoological
Institute and Museum, Biozentrum Grindel, University of Hamburg, D-20146 Hamburg, Germany, and
c
Department of General and Systematic Zoology, Zoological Institute and Museum, Ernst-Moritz-ArndtUniversität, Johann-Sebastian-Bach-Str. 11/12, D-17489 Greifswald, Germany
a
Behavioral studies of sexual selection tend to focus on events that lead up to copulation and the transfer of sperm. Not
surprisingly, we know most about how the selective forces prior to copulation act on female choice and male–male competition.
The playground for postcopulatory processes is the female genital tract where we expect male and female adaptations to control
fertilization. Because postcopulatory processes are hidden away within the female reproductive tract, there are only few systems
(e.g., some birds and insects) where they are well understood. In spiders, studies have revealed an astonishing diversity in
precopulatory selection processes with female choice and male–male competition the focus of investigations. Recent work on
sperm morphology, seminal fluids, and the fertilization process in spiders has highlighted an astonishing and clearly underappreciated diversity. The aim of this ‘‘Ideas’’ paper is to bring together recent advances in sperm and genital morphology with
behavioral studies of sexual selection in spiders. By combining these 2 fields, we aim to identify patterns linking pre and
postcopulatory process and highlight the power of combining morphological and behavioral studies. Key words: accessory gland,
cryptic female choice, sperm activation, sperm competition, spermatheca, sexual selection. [Behav Ecol 22:692–695 (2011)]
INTRODUCTION
exual selection results from the differential reproductive
success between individuals (Darwin 1871) and is largely
responsible for the evolution of numerous behavioral,
morphological, and physiological traits (Andersson 1994).
Up until 30 years ago, it was thought that sexual selection only
occurred at the precopulatory phase (Birkhead and Pizzari
2002; Birkhead 2010). Not surprisingly, the main precopulatory mechanisms, competition for mates and mate choice,
have received intense research attention (Huber 2005; Hunt
et al. 2009). Due to female promiscuity and sperm storage,
however, sexual selection also extends into the postcopulatory
phase within the female genital tract (Birkhead and Pizzari
2002). Postcopulatory sexual selection may act on male and
female characteristics such as sperm traits (see Snook 2005)
and male accessory gland secretions (Gillott 2003) or female
morphology and sperm selection (Eberhard 1996).
The outcome of these pre- and postcopulatory processes is
fertilization success, and there is overwhelming evidence,
especially in insects, that the sperm of some males are more
likely to fertilize a female’s eggs than that of others (Simmons
2001). However, it is not always clear how the processes during
both episodes of sexual selection might interact to produce
the observed paternity patterns. Yet, it is precisely this information that we need in order to understand the evolution of
reproductive strategies (Birkhead and Pizzari 2002; Thomas
and Simmons 2009).
More recently, studies have started to link pre- and postcopulatory processes (Bretman et al. 2006; Koh et al. 2009;
Thomas and Simmons 2009). For example, the precopulatory
mate preferences of female fireflies (Photinus greeni) are re-
S
Address correspondence to M.E. Herberstein. E-mail: marie.
[email protected].
Received 12 December 2010; revised 4 March 2011; accepted 14
March 2011.
Ó The Author 2011. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
lated to the proportion of paternity in double matings with
attractive and unattractive males. Contrary to expectation,
those males that are preferred in precopulatory choices have
lower paternity (Demary and Lewis 2007). Understanding the
actual fertilization processes, which underlie postcopulatory sexual selection, is necessary to understand data like
these. In their elegant morphology-based study, Sbilordo
et al. (2009) show that female yellow dung flies (Scathophaga
stercoraria) control the rate of sperm release from the spermatheca, utilizing sperm more efficiently when it is limited.
This mechanism is likely to explain the greater female
effects on paternity observed in second clutches compared
with first clutches (Sbilordo et al. 2009). Similarly, in situ
observation of the female reproductive tract in a polyandrous moth revealed that contractions of the spermatheca
eject around 50% of sperm from the first mate, explaining
the strong last male precedence (Xu and Wang 2010). Using transgenic Drosophila males with red or green labeled
sperm, Manier et al. (2010) were able to observe competing
sperm within the female tract and reveal the complexity of
the in vivo processes that influence fertilization patterns, including interactions between the female and the ejaculate,
between ejaculates as well as complex sperm behavior.
The examples above highlight that a detailed understanding of
the sperm storage and fertilization process within the female is
required to link pre- and postcopulatory mechanisms and fully
interpret paternity patterns. This can best be achieved by synthesizing insights from several areas of research that have progressed
relatively isolated, specifically the fields of morphology and behavior. In this ‘‘Ideas’’ paper, we want to champion such a synergy
by highlighting recent developments in morphology and behavior. We have chosen to build our argument around spiders, as
they are a significant model organisms in developing ideas surrounding postcopulatory mechanisms (Austad 1984; Eberhard
1996) and exhibit several intriguing features in their reproductive biology, such as their genital and sperm morphology that
Forum: Ideas
challenge current theory (see also Eberhard 2004; Schneider
and Andrade 2011).
LINKING MORPHOLOGY AND BEHAVIOR TO EXPLAIN
PATERNITY OUTCOMES
Using a well-developed model system, the orb web spider
Argiope, we want to illustrate the importance of detailed morphological studies in interpreting paternity patterns derived
from sperm competition experiments. The first paternity
study in this genus (Elgar et al. 2000) revealed that while
highly variable, on average, the first and second male shared
paternity equally (P2—proportion of eggs fertilized by the
second male ;50%). Subsequent sperm competition studies
in congeners established similar patterns (Schneider et al.
2006). Both studies found a relationship between copulation
duration and paternity success. Longer copulations or multiple insertions by the first male decreased P2. These paternity
patterns suggest a standard sperm competition scenario
where copulation duration is related to sperm transfer and
sperm compete with each other following a fair raffle model
(Parker and Simmons 1991). However, details of male and
female genital morphology, described below, reveal the true
complexity of this system.
In most entelegyne spiders (e.g., orb web spiders, jumping
spiders, and wolf spiders), female genitalia are bilaterally
symmetrical with paired copulatory openings, each leading
into separate sperm storage organ. The sperm of 2 males
could be therefore stored separately, avoiding direct sperm
competition, as assumed by most sperm competition scenarios. Furthermore, males transfer their sperm indirectly
via paired pedipalps. Genital damage in male spiders is surprisingly common in araneoid spiders, including in the genus Argiope (Miller 2007). Males break off parts or the entire
pedipalp, which then becomes lodged as a plug in the female
genitalia, preventing another male from utilizing this copulatory opening (Nessler et al. 2007; Foellmer 2008; Uhl et al.
2010). By incorporating this morphological information, the
observed paternity patterns in Argiope (Elgar et al. 2000;
Schneider et al. 2006) are likely the result of the sperm of
each male stored separately. Whether or not sperm of males
can interact in the spermatheca does affect paternity patterns in some orb web spider (Jones and Elgar 2008), although precise mechanisms are unknown. Storage in
different sites provides the female with a relatively easy mechanism to favor ejaculates of 1 male over another by selectively
storing, activating, or utilizing sperm of one or the other spermatheca (Hellriegel and Ward 1998). Indeed A. bruennichi
females favor males that provided longer courtship by allowing them greater paternity shares (Schneider and Lesmono
2009). Furthermore, female A. lobata store less sperm from
related males if they fill the second spermatheca (Welke and
Schneider 2009).
Another intriguing aspect of spider reproductive biology is
that spider sperm is coiled and encapsulated in a sheath in the
male reproductive tract (Alberti 1990; Michalik, Haupt, and
Alberti 2004; Michalik 2007) (Figure 1). After a detour
through the male sperm storage sites within the pedipalps,
this transfer form of sperm arrives in its inactive state in the
female spermathecae (Figure 1). Thus, unlike other animals,
uptake of sperm into the spermatheca is unaffected by sperm
mobility (Eberhard 2004) and in order to be able to swim,
sperm have to shed the capsule and uncoil. Because the processes of decapsulation and uncoiling are separated in time
(e.g., A. bruennichi; Vöcking O, Uhl G, Michalik P, unpublished data), full activation of the spermatozoa seems to require a cascade of signals. Glands associated with female
sperm storage organs in spiders produce secretions that host
693
the sperm and may function partly as a simple matrix (Uhl
1994a; Michalik, Reiher, et al. 2005). However, the complexity
of glandular units suggests that different products are produced at different times (Uhl 1994b, 2000), possibly providing
a cascade of triggers for decapsulation and uncoiling of sperm
(see Figure 1, for a summary). Thus, when considering the
variability of paternity patterns described above, they can be
the result of females selectively activating sperm of one
spermatheca over the other (each containing the sperm of
a different male). Alternatively, sperm in both spermathecae
may be activated simultaneously, thereby triggering sperm
competition in the female fertilization duct.
Understanding the precise mechanisms of sperm activation
is crucial as it will elucidate the level of cryptic female sperm
choice. Interactions between female secretions and male secretions within the ejaculate may extend the possibilities of choice
and manipulation in this dynamic system. Once the sperm are
activated, they need to travel at least through the fertilization
duct, suggesting that sperm traits such as swimming speed are
crucial at this point (Snook 2005). The part of the oviduct to
which the fertilization duct connects (uterus externus) is
generally considered the fertilization site (Foelix 1996), but
supporting data are lacking. There is considerable evidence
that fertilization could also occur in the oviducts or the ovaries
(e.g., Suzuki 1995; Burger et al. 2006). Depending on the site
of fertilization, we can expect specific adaptations in sperm:
Sperm may race toward the ovaries as shown for some mites
(Alberti and Coons 1999), they may wait at specific sites to
meet the eggs, or fertilization may even occur outside the
female’s body shortly after egg laying. As a consequence,
different mechanisms of cryptic female choice and male manipulation are conceivable.
Recent work on sperm morphology in spiders (Michalik et al.
2003, 2006; Michalik, Dallai, et al. 2004; Michalik, Haupt, and
Alberti 2004; Michalik and Alberti 2005; Michalik, Knoflach,
et al. 2005; Michalik and Huber 2006) has highlighted an
astonishing diversity in different organizational levels (e.g.,
sperm conjugations; see also Higginson and Pitnick 2011),
which is not understood especially in the context of sexual
selection. Apart from so-called cleistospermia, where each
sperm is enclosed and transferred individually, spider sperm
can be transferred in aggregates of 2 and more individual
sperm encapsulated by a common secretion sheath (coenospermia). Furthermore, several sperm cells can be completely
fused and encapsulated within a common sheath (synspermia),
a condition only present in some haplogyne spiders (Alberti
and Weinmann 1985; Michalik, Dallai, et al. 2004) and 1 family
of mites (Saxidromidae, Alberti et al. 2007, 2010). Comparative
analyses revealed that cleistospermia are derived and found in
clades such as orb web spiders or jumping spiders (Araneomorphae), whereas coenospermia are plesiomorphic and found
almost exclusively in basal groups such as the bird eating spiders (Mygalomorphae) (Alberti et al. 1986; Michalik, Haupt,
and Alberti 2004). In order to identify the adaptive value of
these sperm transfer forms and their influence on the outcome
of sperm competition, research on the reproductive biology of
those groups is needed. According to Higginson and Pitnick
(2011) sperm conjugations might be a trait selected on the
level of the male, similar to other traits such as accessory gland
proteins or ejaculate size. Although the seminal components
have so far not been identified for spiders, a recent comparative morphological analysis revealed considerable structural diversity of seminal secretion (Michalik 2009). Although no
genital accessory glands are present, male spiders are able to
produce secretion in the testis and/or deferent duct, with one
or several types of seminal secretion present (e.g., Pholcidae:
Michalik and Uhl 2005; Michalik and Huber 2006). There is
also recent indirect behavioral evidence that seminal secretions
Behavioral Ecology
694
Figure 1
Schematic illustration of the
transformation of the sperm
cell in spiders. In the male testes, the sperm is coiled and is
later encapsulated in the deferent ducts. Seminal secretions are produced in the
testes and deferent ducts. After transfer to the female spermatheca, under the possible
influence of male seminal secretions and female spermathecal gland secretions, the
sperm cell is decapsulated
and activated.
in spiders influence fertilization success (Aisenberg and Costa
2005), but direct evidence is still lacking. At the level of sperm
cell organelles in spiders, the acrosome, nucleus, and axoneme
show further structural diversity, which is also not understood. For example, the axoneme of sheet web spiders and
relatives (Linyphioidea: Alberti 1990; Michalik and Alberti
2005; Michalik and Hormiga 2010) lost the central tubules
resulting in a synapomorphic 910 pattern. It is known from
other animal groups that a loss of the central tubules has an
influence on the beating pattern of the sperm tail and is thus
most likely related to traits influenced by sperm competition
(see discussion in Michalik and Alberti 2005).
In addition to interpreting paternity patterns, detailed morphological observations also allow us to predict precopulatory
behavior, thus linking pre- and postcopulatory episodes. For
example, the relationship between sperm transfer rate and copulation duration is likely to be different in conditions of cleistospermia than of coenospermia. Transferring sperm in packages
requires larger diameters of ducts and transfer speed may reach
an upper limit sooner than if smaller, individual gametes are
passed. Sexual conflict over the duration of copulation, if present, will likely take different evolutionary routes, and we would
expect to see different male and female behavioral and morphological adaptations to control copulation duration.
We want to close with 2 simple suggestions. First, we argue
that the combination of behavioral studies linked with
detailed morphological investigations is crucial in further
developing our understanding of the outcomes of pre- and
postcopulatory sexual selection. There are countless published morphological descriptions that linger in journals that
behavioral ecologists typically do not access—this is an untapped resource that we should utilize more intensely.
Second, we hope to remind researchers that those model
systems on which ideas of pre- and postcopulatory sexual
selection are based are just as exceptional as any other mat-
ing system. It is in embracing this diversity that our insights
will fully develop.
We would like to thank 2 anonymous referees and Rob Brooks for
their helpful comments.
REFERENCES
Aisenberg A, Costa FG. 2005. Females mated without sperm transfer
maintain high sexual receptivity in the wolf spider Schizocosa
malitiosa. Ethology. 111:545–558.
Alberti G. 1990. Comparative spermatology of Araneae. Acta Zool
Fenn. 190:17–34.
Alberti G, Afzelius BA, Lucas SM. 1986. Ultrastructure of spermatozoa
and spermatogenesis in bird spiders (Theraphosidae, Mygalomorphae, Araneae). J Submicrosc Cytol Pathol. 18:739–753.
Alberti G, Coineau Y, Fernandez NA, Théron PD. 2010. Fine structure
of the male genital system, spermatophores and unusual sperm cells
of Saxidromidae (Acari, Actinotrichida). Acarologia. 50:243–256.
Alberti G, Coons LB. 1999. Acari—mites. In: Harrison FW, editor.
Microscopic anatomy of invertebrates. Vol. 8c. New York: Wiley-Liss.
p. 515–1265.
Alberti G, Fernandez NA, Coineau Y. 2007. Fine structure of spermiogenesis, spermatozoa and spermatophore of Saxidromus delamarei
Coineau, 1974 (Saxidromidae, Actinotrichida, Acari). Arthropod
Struct Dev. 36:221–231.
Alberti G, Weinmann C. 1985. Fine structure of spermatozoa of some
labidognath spiders (Filistatidae, Segestriidae, Dysderidae, Oonopidae, Scytodidae, Pholcidae; Araneae; Arachnida) with remarks on
spermiogenesis. J Morphol. 185:1–35.
Andersson M. 1994. Sexual selection. Princeton (NJ): Princeton University Press.
Austad SN. 1984. Evolution of sperm priority patterns in spiders. In:
Smith RL, editor. Sperm competition and the evolution of animal
mating systems. New York: Academic Press. p. 223–249.
Birkhead TR. 2010. How stupid not to have thought of that: postcopulatory sexual selection. J Zool. 281:78–93.
Forum: Ideas
Birkhead TR, Pizzari T. 2002. Postcopulatory sexual selection. Nat Rev
Genet. 3:262–273.
Bretman A, Rodrı́guez-Muñoz R, Tregenza T. 2006. Male dominance
determines female egg laying rate in crickets. Biol Lett. 2:409.
Burger M, Michalik P, Graber W, Jacob A, Nentwig W, Kropf C. 2006.
The complex genital system of a haplogyne spider (Arachnida,
Araneae, Tetrablemmidae) indicates internal fertilization and full
female control over transferred sperm. J Morphol. 267:166–186.
Darwin C. 1871. The descent of man and selection in relation to sex.
London: John Murray.
Demary KC, Lewis SM. 2007. Male courtship attractiveness and paternity success in Photinus greeni fireflies. Evolution. 61:431–439.
Eberhard WG. 1996. Female control: sexual selection by cryptic
female choice. Princeton (NJ): Princeton University Press.
Eberhard WG. 2004. Why study spider sex: special traits of spiders
facilitate studies of sperm competition and cryptic female choice.
J Arachnol. 32:545–556.
Elgar MA, Schneider JM, Herberstein ME. 2000. Female control of
paternity in the sexually cannibalistic spider Argiope keyserlingi. Proc
R Soc Lond B Biol Sci. 267:2439–2443.
Foelix R. 1996. Biology of spiders. Oxford: Oxford University Press.
Foellmer MW. 2008. Broken genitals function as mating plugs and
affect sex ratios in the orb-web spider Argiope aurantia. Evol Ecol
Res. 10:449–462.
Fromhage L, Elgar MA, Schneider JM. 2005. Faithfulness without care:
the evolution of monogyny. Evolution. 59:1400–1405.
Gillott C. 2003. Male accessory gland secretions: modulators of female
reproductive physiology and behavior. Annu Rev Entomol. 48:163–184.
Hellriegel B, Ward PI. 1998. Complex female reproductive tract morphology: its possible use in postcopulatory female choice. J Theor
Biol. 190:179–186.
Higginson DM, Pitnick S. 2011. Evolution of intra-ejaculate sperm
interactions: do sperm cooperate? Biol Rev. 87:249–270.
Huber BA. 2005. Sexual selection research on spiders: progress and
biases. Biol Rev. 80:363–385.
Hunt J, Breuker CJ, Sadowski JA, Moore AJ. 2009. Male-male competition, female mate choice and their interaction: determining total
sexual selection. J Evol Biol. 22:13–26.
Jones TM, Elgar MA. 2008. Male insemination decisions and sperm
quality influence paternity in the golden orb-weaving spider. Behav
Ecol. 19:285–291.
Koh T, Seah W, Yap L-M, Li D. 2009. Pheromone-based female mate
choice and its effect on reproductive investment in a spitting spider.
Behav Ecol Sociobiol. 63:923–930.
Manier MK, Belote JM, Berben KS, Novikov D, Stuart WT, Pitnick S.
2010. Resolving mechanisms of competitive fertilization success in
Drosophila melanogaster. Science. 328:354–357.
Michalik P. 2007. Spermatozoa and spermiogenesis of Liphistius cf.
phuketensis (Mesothelae, Araneae, Arachnida) with notes on phylogenetic implications. Arthropod Struct Dev. 36:327–335.
Michalik P. 2009. The male genital system of spiders (Araneae) with
notes on the fine structure of seminal secretions. Contrib Nat Hist
Bern. 12:959–972.
Michalik P, Alberti G. 2005. On the occurence of the 910 axonemal
pattern in the spermatozoa of sheetweb spiders (Araneae, Linyphiidae). J Arachnol. 33:569–572.
Michalik P, Dallai R, Giusti F, Alberti G. 2004. The ultrastructure of the
peculiar synspermia of some Dysderidae (Araneae, Arachnida). Tissue Cell. 36:447–460.
Michalik P, Gray MR, Alberti G. 2003. Ultrastructural observations of
spermatozoa and spermiogenesis in Wandella orana Gray, 1994
(Araneae: Filistatidae) with notes on their phylogenetic implications. Tissue Cell. 35:325–337.
Michalik P, Haupt J, Alberti G. 2004. On the occurrence of coenospermia in mesothelid spiders (Araneae: Heptathelidae). Arthropod
Struct Dev. 33:173–181.
Michalik P, Hormiga G. 2010. Ultrastructure of the spermatozoa in
the spider genus Pimoa: new evidence for the monophyly of
695
Pimoidae plus Linyphiidae (Arachnida: Araneae). Am Mus
Novit. 3682:1–17.
Michalik P, Huber BA. 2006. Spermiogenesis in Psilochorus simoni
(Berland, 1911) (Pholcidae, Araneae): evidence for considerable
within-family variation in sperm structure and development. Zoology.
109:14–25.
Michalik P, Knoflach B, Thaler K, Alberti G. 2005. The spermatozoa of
the one-palped spider Tidarren argo (Araneae, Theridiidae). J Arachnol. 33:562–568.
Michalik P, Reiher W, Suhm-Tintelnot M, Coyle FA, Alberti G. 2005.
The female genital system of the folding-trapdoor spider Antrodiaetus
unicolor (Hentz, 1842) (Antrodiaetidae, Araneae) - an ultrastructural
study of form and function with notes on reproductive biology of
spiders. J Morphol. 263:284–309.
Michalik P, Sacher P, Alberti G. 2006. Ultrastructural observations
of spermatozoa of several tetragnathid spiders with phylogenetic implications (Araneae, Tetragnathidae). J Morphol. 267:
129–151.
Michalik P, Uhl G. 2005. The male genital system of the cellar
spider Pholcus phalangioides (Fuesslin, 1775) (Pholcidae, Araneae): development of spermatozoa and seminal secretion. Front
Zool. 2:12.
Miller JA. 2007. Repeated evolution of male sacrifice behavior in spiders correlated with genital mutilation. Evolution. 61:1301–1315.
Nessler SH, Uhl G, Schneider JM. 2007. Genital damage in the orbweb spider Argiope bruennichi (Araneae: Araneidae) increases paternity success. Behav Ecol. 18:174–181.
Parker GA, Simmons LW. 1991. A model of constant random sperm
displacement during mating: evidence from Scatophaga. Proc R Soc
Lond B Biol Sci. 246:107–115.
Sbilordo SH, Schäfer MA, Ward PI. 2009. Sperm release and use at
fertilization by yellow dung fly females (Scathophaga stercoraria). Biol
J Linn Soc. 98:511–518.
Schneider JM, Andrade MCB. 2011. Mating behaviour and sexual
selection. In: Herberstein ME, editor. Spider behaviour: flexibility
and versatility. Cambridge (UK): Cambridge University Press.
Schneider JM, Gilberg S, Fromhage L, Uhl G. 2006. Sexual conflict
over copulation duration in a cannibalistic spider. Anim Behav.
71:781–788.
Schneider JM, Lesmono K. 2009. Courtship raises male fertilization
success through post-mating sexual selection in a spider. Proc R Soc
Lond B Biol Sci. 276:3105–3111.
Simmons LW. 2001. Sperm competition and its evolutionary consequences in the insects. Princeton (NJ): Princeton University Press.
Snook RR. 2005. Sperm in competition: not playing by the numbers.
Trends Ecol Evol. 20:46–53.
Suzuki H. 1995. Fertilization occurs internally in the spider Achaearanea tepidariorum (C. Koch). Invertebr Reprod Dev. 28:211–214.
Thomas ML, Simmons LW. 2009. Male dominance influences pheromone expression, ejaculate quality, and fertilization success in the
Australian field cricket, Teleogryllus oceanicus. Behav Ecol. 20:1118–1124.
Uhl G. 1994a. Genital morphology and sperm storage in Pholcus phalangioides (Fuesslin, 1775) (Pholcidae, Araneae). Acta Zool. 75:1–12.
Uhl G. 1994b. Ultrastructure of the accessory glands in female genitalia of Pholcus phalangioides (Fuesslin, 1775) (Pholcidae; Araneae).
Acta Zool. 75:13–25.
Uhl G. 2000. Two distinctly different sperm storage organs in female
Dysdera erythrina (Araneae: Dysderidae). Arthropod Struct Dev. 29:
163–169.
Uhl G, Nessler SH, Schneider J. 2010. Securing paternity in spiders? A
review on occurrence and effects of mating plugs and male genital
mutilation. Genetica. 138:75–104.
Welke K, Schneider JM. 2009. Inbreeding avoidance through cryptic
female choice in the cannibalistic orb-web spider Argiope lobata.
Behav Ecol. 20:1056–1062.
Xu J, Wang Q. 2010. Mechanisms of last male precedence in a moth:
sperm displacement at ejaculation and storage sites. Behav Ecol.
21:714–721.