Genetica

, 138:75

Securing paternity in spiders? A review on occurrence and effects of mating plugs and male genital mutilation

Authors

    • Department of General and Systematic Zoology, Zoological Institute and MuseumUniversity of Greifswald
  • Stefan H. Nessler
    • Biozentrum Grindel, Department of EthologyUniversity of Hamburg
  • Jutta M. Schneider
    • Biozentrum Grindel, Department of EthologyUniversity of Hamburg
Article

DOI: 10.1007/s10709-009-9388-5

Cite this article as:
Uhl, G., Nessler, S.H. & Schneider, J.M. Genetica (2010) 138: 75. doi:10.1007/s10709-009-9388-5

Abstract

Low female mating frequencies often appear to be cases of direct male induction that can oppose female interests. Mating plugs are most obvious means leading to low degrees of multiple mating in females. In spiders, mating plugs are formed by a variety of amorphous materials, by the breakage of the male sperm transferring organ, or by the whole male that functions as a mating barrier. Our compilation of the available information on the presence of the various types of mating plugs suggests that plugs predominantly occur in entelegyne spiders. In this group, plugs do not interfere with oviposition since separate openings for insemination and oviposition are present. In contrast, mating plugs seem to be rare in haplogyne spiders that do not possess separate openings. The available experimental studies on the function of the different types of plugs suggest that plugs can be considered as male adaptations to avoid sperm competition. However, females in some cases were shown to have evolved means to prevent or control male manipulation or may selectively favour plug production in specific males, an aspect which has largely been neglected. In order to understand plug evolution and function we need to explore the morphological, behavioural and biochemical aspects involved and extend our approach to interactions between the sexes.

Keywords

Copulatory plugsSexual selectionSexual conflictAraneaeMate guarding

Introduction

Promiscuity and sperm competition

Sperm competition is undoubtedly a strong selective agent responsible for the evolution of many physiological, behavioural and morphological traits (Parker 1970). These traits are offensive adaptations if they help the male`s sperm to prevail in sperm competition by flushing out, replacing, diluting or displacing the ejaculates of previous males from the sperm storage sites of the female. Defensive adaptations, on the other hand, help to avoid or reduce competition by reducing the probability of female remating by guarding her, by manipulating her willingness to remate, her attractiveness to subsequent males, her willingness to allow flushing out etc., or by applying mechanical barriers impeding access to sperm storage sites (Parker 1970; Simmons 2001). A prime example of an evolutionary adaptation against female multiple mating and sperm competition is a mating plug (copulatory plug) produced by the male and applied to the female copulatory openings after mating (Boorman and Parker 1976; Simmons 2001). Solid material occurs on or in the genital openings of the females following mating in a wide range of animal taxa, including mammals, birds, reptiles and amphibians and especially in insects and arachnids (Drummond 1984; Gomiendo et al. 1998; Wigby and Chapman 2004; Simmons 2001; Eberhard 1996, 2004; Elgar and Schneider 2004). Some or even most of these materials may have evolved under sexual selection as paternity protection devices by preventing or delaying female remating (Parker 1970; Simmons 2001) or by binding up sperm from previous males (Nilakhe and Villavaso 1979). Furthermore, these substances may have cryptic effects on female reproductive physiology and behaviour that favour the male`s reproductive success (Eberhard 1996; Eberhard and Cordero 1995; Arnqvist and Rowe 2005; Wigby and Chapman 2005). However, mating plugs could have other functions that evolved under natural selection, i.e. they may retain sperm in a position where chances are higher that they will be stored or used for fertilization of the eggs (Polak et al. 1998), they may prevent sperm desiccation (Huber 1995), or passive sperm loss through leakage (Hinton 1964). Although we focus this review on mating plugs as mechanical barriers that impede female remating, the alternative, nonexclusive functions under natural selection mentioned above are considered when suggestive evidence is available.

Spider genitalia and their potential for the evolution of mating plugs

In most animal species, a mechanical barrier that prevents a female from remating can only block her genital opening for a limited period of time, since the same opening is also used for oviposition. Long-lasting mating plugs would be detrimental to both sexes since they would prevent the female from ovipositing. However, there are two exceptional taxa: ditrysian Lepidoptera as well as the majority of spiders (Entelegynae) and some mites have evolved more than one genital opening (Alberti and Coons 1999; Drummond 1984; Foelix 1996). These independently evolved anatomical features allow the female to oviposit despite blocked copulatory openings. Female entelegyne spiders usually possess three genital openings: two lateral insemination ducts, each connected to a sperm storage site, and a central opening for oviposition. Sealing one or both of the insemination ducts does not prevent the female from laying fertilized eggs since the spermathecae are connected with the oviduct via fertilization ducts. Moreover, female spiders can store sperm for extended periods of time before it is used for fertilization during an egg-laying bout, from which follows that sperm competition intensity is high if females mate with more than one male and store multiple ejaculates (Austad 1984; Foelix 1996; Uhl 1992). Therefore, males are expected to evolve adaptations that reduce female remating, e.g. via mating plugs and/or seminal proteins (Huber 2005a). Especially in entelegyne spiders, mating plugs that help to secure paternity should be selectively favoured.

On the other hand, females may profit from a mating plug if they have the possibility to mate with a preferred male, thereby securing high quality sperm, preventing loss of sperm, sperm desiccation or infections through an open copulatory duct. Also, at least in some species females are able to influence the efficacy of the plug by contributing secretions themselves. These possibilities have largely been neglected (but see “Female Participation in Plug Production”.)

In spiders, mating plugs can consist of either secretory, amorphous material that is deposited on the entrance of the female copulatory ducts, or of parts of the males’ copulatory organs, the pedipalps, that are left behind in the female genital tract (Fig. 1). In some cases, the whole pedipalp or the male’s soma itself appears to function as a re-mating barrier. There is ample evidence for potential mating plugs in spiders in comments and drawings found scattered throughout the taxonomic literature (Table 1). However, it is often not clear if plugging is frequent or rare in a given species, since mostly only a single or few females were investigated. Furthermore, it is possible that the presence of material at the copulatory openings may be an artefact of the collecting and storing method. On the other hand, female genitalia are generally mechanically or chemically cleaned by taxonomists before studying their morphology, which increases the likelihood of destroying actual plugs. As a consequence, the frequency of amorphous mating plugs and their taxonomic distribution within the Araneae is not yet clear. Likewise, broken male genital structures that are left behind in the female genital tract often only become visible after dissecting and macerating the female genitalia, since the remains are lodged deep inside the copulatory duct or within the spermathecae. Any estimate of the frequency of plugging must therefore be treated with care. Due to the scattered and incomplete information, a phylogenetic interpretation on the occurrence of mating plugs in spiders is premature. However, there seem to be only few haplogyne but relatively many entelegyne spiders for which mating plugs are reported (Table 1), suggesting that indeed entelegyne female genitalia resulted in numerous cases of convergent evolution of various kinds of mating plugs.
https://static-content.springer.com/image/art%3A10.1007%2Fs10709-009-9388-5/MediaObjects/10709_2009_9388_Fig1_HTML.jpg
Fig. 1

Different kinds of mating plugs found in epigynes of females in selected species. AD Epigynes with broken-off genital parts; scale bars 500 μm, EH genital openings sealed with amorphous secretions. A Macerated epigyne of Argiope bruennichi. The arrow indicates the short broken-off embolus tip stuck in the insemination duct. Phot: S. H. Nessler B Macerated epigyne of A. aurantia with several broken-off emboli inside the atrium. Phot: S. H. Nessler CA. lobata epigyne with a protruding embolus (white arrow). Phot: S. H. Nessler DNephila fenestrata female with two embolic conductors inside her genital openings (white arrows). Phot: L. Fromhage EFOedothorax retusus with small (E) and big (F) plug (white arrow); scale bar = 40 μm. Phot: K. Kunz. GHArgyrodes (fissifrontellus) before mating (G) and after mating (H). The genital openings (Gwhite arrows) are covered with amorphous secretion after mating (Hwhite arrows). Scale bars 100 μm. Phot: G. Uhl

Table 1

Compilation of information available on the existence, type, frequency and effect of a mating plug that is formed by amorphous material (A) or through genital mutilation of the male (M)

Family

Genus species

Type

Origin

Frequency

Barrier

References

Agelenidae

Agelenalabyrinthica, limbata

A

Female secretions/male palpal glands

High

Yes

Strand (1906); Menge (1868); Masumoto (1993); Roberts (1993)

 

Agelenopsiskastoni, oklahoma

M

Embolus

Often

?

Gering (1953)

 

Neoramianana

A

?

?

?

M. J. Ramírez, personal communication (2008)

 

Tegenarialabyrinthi

A

?

?

?

A. Bolzern, personal communication (2008)

 

Malthonicasilvestris

A

?

?

?

A. Bolzern, personal communication (2008)

Amaurobiidae

Amaurobiusfenestralis, ferox

A

Male bulbal gland

High

Possible

Gerhardt (1923, 1924); Wiehle (1953); Suhm (1992); Suhm and Alberti (1993); Suhm et al. (1996), G. Alberti, personal communication (2008)

 

Pimusnapa

A

?

?

?

M. J. Ramírez, personal communication (2008)

Amphinectidae

Tasmarubriushickmani, milvinus, pioneer, tarraleah, truncus

A

?

High

?

Davies (1998)

 

Tanganagreeni

A

?

Often

?

Davies (2003b)

 

Tasmabrochuscranstoni

A

?

?

?

Davies (2002)

Anyphaenidae

Gamakiahirsuta

A

?

Often

?

Ramírez (2003)

 

Axyracruselegans

A

?

Often

?

Ramírez (2003)

 

Malenella spp.

A

?

?

?

Ramírez (2003)

 

Monapia spp.

A

?

High

?

Ramírez (1999, 2003)

Araneidae

Acacesiahamata

M

Scale on embolus

High

Possible

Levi (1976)

 

Aculepeirapackardi

M

Embolus cap

?

?

 
 

Acusilas spp.

M

Embolus

High

?

N. Scharff, personal communication (2008)

 

Araneusmineatus & juniperi group

A

?

High

Possible

Gertsch (1979)

 

Araneusalsine, angulatus, bispinosus, calusa, cavaticus, cingulatus, cochise, corporosus, corticarius, cristobal, detrimentosus, diadematus, gadus, gemma, gemmoides, groenlandicola, guttulatus, illaudatus, ivei, mammatus, marmoreus, mendoza, miniatus, missouri, monica, montereyensis, nashoba, nordmanni, pallidus, partitus, popaco, quadratus, saevus, texanus, thaddeus, trifolium, washingtoni, workmani, yukon

M

Embolus cap

High

Possible

Wiehle (1967a); Grasshoff (1968); Levi (1970, 1971c, 1973, 1975a, 1991); Scharff and Coddington (1997)

 

Argiopeaemula, aetheroides, amoena, argentata, aurantia, blanda, bruennichi, dietrichae, flavipalpis, katherina, keyserlingi, lobata, magnifica, niasensis, ocula, ocyaloides, pulchella, pulchelloides, radon, savignyi, sector, taprobanica, trifasciata, versicolor

M

Part of embolus

Often/high

?/yes

Abalos and Baez (1963); Levi (1965, 1968, 1970, 1975a, 1983, 2004); Edmunds (1982); Yin et al. (1989); Scharff and Coddington (1997); Kuntner (2005); Nessler et al. (2007a, b); Foellmer (2008); Kuntner et al. (2008); Nessler et al. (2009); S. H. Nessler, unpublished; G. Uhl, unpublished

 

Aspidolasiusbranicki

M

Part of embolus

High

Possible

Calixto and Levi (2006)

 

Caerostriscorticosa,mitralis, sexcuspidata, sumatrana, vicina

M

Part of embolus

High

Possible

Grasshoff (1984); Jäger (2007); Kuntner et al. (2008)

 

Cyclosa spp., diversa, fililineata, nevada, ojeda, tamanaco

M

Part of embolus/tooth of conductor

?/rare/often

Possible

Levi (1999), Kuntner et al. (2008)

 

Deilochus spp., zelivira

M

Embolus and embolic conductor

?

?

Kuntner (2005); Miller (2007); Kuntner et al. (2008)

 

Hyposingaalberta, albovittata, funebria, groenlandicola, pygmaea, rubens, sanguinae, funebris

M

Scale of embolus

High

Possible

Locket and Millidge (1953); Holm (1959); Levi (1971a, b); Roberts (1993); Miller (2007); Y. Marusik, personal communication (2008)

 

Kilimagriseovariegata, conspersa

M

Tip of embolus

High

Possible

Grasshoff (1970a)

 

Lariniabifida, borealis, chloris, directa, famulatoria, trifida

M

Embolus tip/cap

?/high

Possible

Levi (1975b); Grasshoff (1970b, 1971); Scharff and Coddington 1997; Y. Marusik, personal communication (2008)

 

Manogeagaira

M

Embolus piece

High

Possible

Levi (1997)

 

Metazygiaerratica

A

?

High

Possible

Levi (1995a)

 

Metazygiazilloides

M

Part of embolus

?

?

Levi (1995a)

 

Metepeira spp., arizonica, labyrinthea

AM

Embolus cap

Often/high

Possible

Abalos and Baez (1963); Levi (1977); Scharff and Coddington (1997); Piel (2001)

 

Milonia spp., brevipes, obtusa

M

Part of embolus

?/high

?

N. Scharff, personal communication (2008); V. Framenau, personal communication (2008)

 

Neogeanoticolor

M

Embolus tip

?

?

Levi (1983)

 

Ocrepeiraalbopunctata

M

Embolus scale

High

Possible

Levi (1993)

 

Phonognathamelanopyga

M

Embolic conductor and embolus

?

Possible

Kuntner et al. (2008)

 

Singafrotypaokavango

M

Embolus scale

Often

Possible

Kuntner and Hormiga (2002)

 

Spintharidiusrhomboidalis

M

Embolus appendage

High

Possible

Levi (1995b, 2008)

 

Wagnerianatauricornis

M

Embolus caps

High

Possible

Levi (1976)

 

Witica spp.

M

Part of embolus

?

?

Levi (1986)

Clubionidae

spp.

A

?

Often

?

Forster (1967)

 

Clubionabrevipes

M

pedipalp

?

?

Wiehle (1960, 1967a)

 

Elavercf. tigrinella

A

?

?

?

M. J. Ramírez, personal communication (2008)

Corinnidae

spp.

A

?

?

 

P. Lehtinen, personal communication (2008)

 

Brachyphaeasimoni

A

?

?

?

M. J. Ramírez, personal communication (2008)

 

Castianeiratrilineata

A

?

?

?

M. J. Ramírez, personal communication (2008)

 

Copaflavoplumosa

A

?

?

?

M. J. Ramírez, personal communication (2008)

 

Mandanetasudana

A

?

?

?

M. J. Ramírez, personal communication (2008)

 

Otacilia sp.

A

?

?

?

M. J. Ramírez, personal communication (2008)

 

Paccius spp., cf. scharffi

A

tibial setae?

Often

?

Platnick (2000b); M. J. Ramírez, personal communication (2008)

 

Phrurolithusclaripes, festivus

A

?

?

?

Kaston (1981); Marusik and Crawford (2006); M. J. Ramírez, personal communication (2008)

Phrurotimpus alarius

A

?

?

?

M. J. Ramírez, personal communication (2008)

 

Procopiuscf. aethiops

A

?

?

?

M. J. Ramírez, personal communication (2008)

Ctenidae

Antisiratenusnov.gen.

A

?

Often

Possible

D. Silva-Dávila, personal communication (2008)

 

Amauropelmaundara

A

?

?

?

Raven et al. (2001)

 

Ctenusmirificus

A

?

Often

Possible

Steyn et al. (2002)

 

Mahafalytenusfohy

A

?

Often

Possible

Silva-Dávila (2007)

 

Phoneutrianigriventer

A

¿

Often

Possible

A. J. Santos, personal communication (2009)

Cybaeidae

Cybaeusjinsekiensis, kokuaensis, kuramotoi

M

Embolus tip

High

Possible

Ihara (2006, 2007)

Cycloctenidae

Cycloctenusnelsonensis

A

?

?

?

M. J. Ramírez, personal communication (2008)

 

Toxopsiellaminuta

A

?

?

?

M. J. Ramírez, personal communication (2008)

Desidae

spp.

A

?

?

?

Forster (1967)

Dictynidae

Argennasubnigra

A

Male secretion

Rare/high

Possible

Bertkau (1889); Gerhardt (1923); Wiehle (1953); Roberts (1993)

 

Dictynauncinata

M

Part of embolus

Often

Possible

Wiehle (1967a)

 

Mastigusaarietina

M

Whole palp

Often

?

Bertkau (1894)

 

Lathysstigmatisata group

M

Part of embolus

?

Possible

Wiehle (1967a); Marusik et al. (2006); Y. Marusik, personal communication (2008)

Gallieniellidae

Meedogympie

M

Part of embolus

Often

Unlikely

Platnick (2002)

Gnaphosidae

spp.

A

?

?

?

Grimm (1985), Suhm et al. (1995)

 

Berlandinanubivaga

A

?

?

?

Grimm (1985)

 

Gnaphosalucifuga

A

?

?

Possible

Uhl and Gack, unpublished

 

Haplodrassus spp.

A

?

?

?

R. Bosmanns, personal communication (2008); Y. Marusik, personal communication (2008)

 

Haplodrassussignifier, dalmatensis

A

?

?

?

Roberts (1993); Uhl and Gack, unpublished

 

Micariaaenea, alpina

A

?

?

?

Mikhailov and Marusik (1991); Y. Marusik, personal communication (2008)

 

Trachyzelotesbarbatus

A

?

?

?

J. Wunderlich, personal communication (2008)

 

Xenoplectus sp.

A

?

?

?

M. J. Ramírez, personal communication (2008)

Idiopidae

Neoctenizaaustralis, minima, platnicki

M

Embolus tip

Often

Possible

Goloboff (1987)

Lamponidae

Bigendita spp.

A

?

High

Possible

Platnick (2000a)

 

Centrocalia spp.

A

?

Often

Possible

Platnick (2000a)

 

Centrothele spp., mutica

A

?

Often

Possible

Platnick (2000a); M. J. Ramírez, personal communication (2008)

 

Lamponacylindrata, murina

A

?

High

Possible

Platnick (2000a)

Linyphiidae

Ceratinellabrevis

A

?

?

Unlikely

Uhl and Gack, unpublished

 

Dicymbiumnigrum

M

Conductor and embolus

?

Possible

Cambridge (1871)

 

Diplothyroncf

A

?

High

Unlikely

Berghammer (cit. Eberhard 1996)

 

Dubiaraneaabjecta, affinis, atripalpis, fulvolineata, fusca, insula, margaritata, signifera

A

?

Rare

Possible

Millidge (1991)

 

Linyphiatriangularis

A

?

High

Possible

Stumpf and Linsenmair (1996)

 

Mermessuscontorta, tenuipalpis, tridentatus, trilobatus

A

?

High

Possible

Edwards (1993); Uhl and Gack, unpublished; M. H. Schmidt-Entling, personal communication (2008); A. Hänggi, personal communication (2008), Uhl, unpublished

 

Minyrioluspusillus

M

Embolus

?

?

Wiehle (1967a)

 

Novafrontinauncata

A

?

Often

?

Millidge (1991)

 

Oedothoraxretusus

A

Male palp

98%

Yes

Uhl and Busch (2009)

 

Pityohyphantesphrygianus

A

Male palp

High

?

Uhl and Gunnarsson (2001)

 

Prinerigonevagans

A

?

High

Possible

Roberts (1993)

 

Walckenaeriastylifrons

M

Part of embolus

?

?

Wunderlich (1972)

Liocranidae

Agroecabrunnea, cuprea, lusatica

A

?

Often

?

Roberts (1993); C. Szinetár, personal communication (2008); R. Bosmans, personal communication (2008); M. J. Ramírez, personal communication (2008), Uhl, unpublished

 

Apostenusannulipedes, californicus, fuscus, gomerensis, grancanariensis

A

?

Often

Possible/easy to remove

Grimm (1986); Wunderlich (1987, 1992); Roberts (1993); M. J. Ramírez, personal communication, (2008)

 

Liocranoecastriata

A

?

?

Easy to remove

R. Bosmans, personal communication (2008)

Lycosidae

spp.

A

?

?

?

Suhm et al. (1996) as personal observation

 

Alopecosapsammophila

A

?

?

?

Szinetár et al. (2005)

 

Hogna spp., albemarlensis

A

?

?

?

J.-P. Maelfait and C. De Busschere, personal communication (2008)

 

Pardosa(Wadicosa) oncka

A

?

High

Possible

Kronestedt (1987)

 

Trochosaruricola

A

?

?

?

M. J. Ramírez, personal communication (2008)

 

Wadicosafidelis

A

 

?

?

T. Kronestedt, personal communication (2008)

Miturgidae

Cheiracanthiumafricanum, furculatum, inclusum

A

?

Often/high

Possible

Bonaldo and Brescovit (1992); A. Brescovit, personal communication (2008); L. Lotz, personal communication (2008); M. J. Ramírez, personal communication 2008

 

Cheiracanthiumerraticum

M

Part of embolus

?

?

Wiehle 1967a

 

Cheiramiona spp.

A

?

?

?

M.J. Ramírez, personal communication 2008; L. Lotz, personal communication 2008

 

Eutichurus spp.

A

?

Often

?

Bonaldo 1994

 

Macerioflavus

A

?

?

?

Ramírez et al. 1997

 

Radulphius spp.

A

?

Often

?

Bonaldo 1994

 

Systarialongipes

A

?

?

?

M.J. Ramírez, personal communication 2008

Mysmenidae

Calodipoenaincredula

M

Part of embolus

Often

?

Levi 1956

Nephilidae

Herenniaagnarssoni, deelemanae, etruscilla, gagamba, milleri, multipuncta, oz, papuana, tone

M

Part of embolus and embolic conductor

High

Possible

Robinson and Robinson 1978; Levi and von Eickstedt 1989; Kuntner 2005; Kuntner et al. 2008

 

Nephilaclavipes, constricta, fenestrata, inaurata “komaci”, madagascariensis, plumipes, senegalensis, turneri

M

Part of embolus and embolic conductor

Often/high

Yes/no

Bertkau 1894; Wiehle 1960, 1967a; Müller 1982; Schult and Sellenschlo 1983; Schneider et al. 2001; Kuntner 2005; Schneider et al. 2005b; Fromhage and Schneider 2006; Kuntner et al. 2008

 

Nephilapilipes

AM

?/part of embolus and embolic conductor

Often/high

?

Robinson 1982; Kuntner et al. 2009a

 

Nephilengysborbonica, cruentata, malabarensis

M

Part of embolus and embolic conductor

Often

No

Cambridge 1871; Göldi 1892; Robinson and Robinson 1978, 1980; Kuntner 2005, 2007; Kuntner et al. 2008; Edmunds personal communication 2008

Nesticidae

Nesticuscellulanus

A

?

High

?

Weiss 1981; B. A. Huber personal communication 2009

Oxyopidae

Oxyopesconstrictus

A

?

Often

?

A. Santos personal communication 2008

 

Peucetiaflava, viridians

AM

?/apex of paracymbium

Absent/often/high

Possible

Petrunkevitch 1929; Brady 1964; Gertsch 1979; Exline and Whitcomb 1965; Whitcomb and Eason 1965; Santos and Brescovit 2003; M. G. Ramírez, personal communication 2009; A. Santos, personal communication (2008)

 

Peucetialongipalpis, rubrolineata

A

?

Often

?

Santos and Brescovit 2003; A. Santos personal communication 2008

 

Peucetiamacroglossa

M

Apex of paracymbium

?

?

Santos and Brescovit 2003

 

Schaenicoscelisleucochlora

M

Apex of male conductor

Often

?

A. Santos, personal communication (2008)

 

Tapinilluslongipes

M

Apex of paracymbium

Often

?

A. Santos, personal communication (2008)

Pisauridae

Architisspinipes, tenuis

A

?

Rare/often

Possible

Santos (2007a, b); A. Santos, personal communication (2008)

 

Dolomedesscriptus, triton, vittatus

M

Embolus tip

Rare

Possible

Carico (1973)

 

Eurychoerabanna

M

Embolus

Often

?

Jäger (2007), Jäger and Praxaysombath (2009)

 

Eurychoeraquadrimaculata

A

?

?

?

Jäger (2007)

 

Thalassiusmajungensis, massajae

M

Piece of embolus

Always

Possible

Sierwald (1984, 1987)

Philodromidae

Philodromusaureolus, praedatus

A

Sperm and (male?) secretions

?

?

Huber (1995); Kubcová (2004)

 

Philodromusdispar, poecilus

M

Embolus tip

Rare

?

C. Muster, personal communication (2008)

 

Tibellusoblongus

A

?

?

?

M. J. Ramírez, personal communication (2008)

Pholcidae

Belisanakhaosok, leuser

A

Sperm and secretion

?

?

Huber (2005b)

 

Carapoiaubatuba

A

?

?

?

Huber (2005c)

Salticidae

Aillutticupinquidor

A

?

?

?

Galiano (1987)

 

Cocalodeslongicornis

A

?

?

?

M. J. Ramírez, personal communication (2008)

 

Euophryssutrix

A

?

High

?

C. Grismado, personal communication (2008)

 

Euryattusmyiopotami

M

Embolus tip

?

?

Proszynski (1984a)

 

Heliophanuscupreus, flavipes

A

?/sperm plug

Often/high

?

Dahl (1926); Harm (1971); Roberts (1993); R. Bosmanns, personal communication (2008); J. Proszynski, personal communication (2008); C. Szinetár, personal communication (2008); Uhl and Gack, unpublished

 

Holcolaetis spp.

A

?

Often

?

Wanless (1985)

 

Menemerusbivittatus

A

?

Rare

?

Chrysanthus (1968)

 

Phidippusjohnsoni, paykulli

A

Male secretions?

Often

Yes

Jackson (1980); Austad (1984); Bohdanowicz and Proszynski (1987)

 

Portiaafricana, albimana, fimbriata, labiata, schultzi

A

?

Often

?

Jackson and Hallas (1986); R. R. Jackson, personal communication

 

Telamoniafestiva

M

Embolus tip

?

?

Proszynski (1984b)

 

Telamoniavlijmi

A

?

?

?

Bohdanowicz and Proszynski (1987)

Sparassidae

Cebrennuspowelli, rungsi

A

?

Often

?

Jäger (2000)

 

Delenacancerides

M

Part of embolus

?

Possible

Järvi (1914)

 

Heteropodabelua

A

?

?

?

Jäger (2005a)

 

Oliosauricomis, lutescens, obesulus, rotundiceps

A

?

?

?

P. Jäger personal communication (2008)

 

Palystescastaneus, hoehneli

A

?

?

?

Jäger and Kunz (2005)

 

Pseudopodalutea

A

?

?

?

Jäger (2002); Jäger and Ono (2002)

 

Rhitymnaoccidentalis, plana, simoni

A

?

?

?

Jäger (2003, 2007)

 

Sinopodaokinawana

A

?

?

?

P. Jäger, personal communication (2008)

 

Spariolenussecundus

A

?

?

?

Jäger (2006)

 

Thelcticopispicta

A

?

?

?

Jäger (2005b)

Stiphidiidae

Boralinae spp.

A

?

Often

?

Gray and Smith (2008); H. Smith and M. Gray, personal communication (2008)

 

Barahnabooloumba

M

Part of embolus

?

Possible

Davies (2003a)

 

Jamberoojohnnoblei

A

?

?

?

Gray and Smith (2008)

 

Karriellatreenensis

A

?

?

?

Gray and Smith (2008)

Synotaxidae

Acrometa? cristata (fossil)

A

?

?

 

Wunderlich (2004)

Tengellidae

Lauriciushooki

A

?

?

?

M. J. Ramírez, personal communication (2008)

 

Liocranoides spp., unicolor

A

?

High

Possible

Platnick (1999); M. J. Ramírez, personal communication (2008)

 

Tengellaperfuga, radiata

A

?

High

?

Platnick (2009); M. J. Ramírez, personal communication (2008)

Tetragnathidae

Leucaugemariana

A

Male palpal and female secretions

High

?

Eberhard et al. (1993); Eberhard and Huber (1998a);

Aisenberg and Eberhard (2009)

 

Leucauge sp.

M

Part of embolus

?

Possible

Wiehle (1967b); Kuntner (2005); Kuntner et al. (2008)

Theridiidae

spp.

A

?

?

?

Forster (1967)

 

Theridiidae(fossil)

A

?

?

?

Wunderlich (2008)

 

Argyrodesantipodianus, argentatus, argyrodes, elevatus, nephilae

A

Sperm plug/femle secretion/male palpal secretion

High

Possible

Strand (1906); Chrysanthus (1963); Petrunkevitch (1930); Gertsch (1979); Exline and Levi (1962); Levi et al. (1982); Whitehouse and Jackson (1994); Knoflach (2004); Uhl, personal observation

 

Chryssocambridgei

A

Male palp or genital tract

High

Yes

Knoflach (2004)

 

Dipoenachillana

A

?

High

Yes

Levi (1963)

 

Echinotheridioncartum

A/M

?/entire male palp

Often/high

?

Ramírez and González (1999)

 

Echinotheridiongibberosum

M

Entire male palp

High

Short term

Ramírez and González (1999); Knoflach (2002)

 

Emertonella

A

?

Often

?

H. Smith, personal communication (2008)

 

Enoplognathaovata group, quadripunctata, serratosignata

A

?

?

?

Huseynov and Marusik, (2007); Y. Marusik, personal communication (2008); R. Bosmans, personal communication (2008)

 

Enoplognathalatimana

M

Tip of conductor

?

?

Wunderlich (1995); J. Wunderlich, personal communication (2008)

 

Euryopis spp., saukea

A

?

?

?

Y. Marusik, personal communication (2008); H. Smith, personal communication (2008)

 

Latrodectusantheratus, corallinus, curacaviensis, dahli, geometricus, hasselti, hesperus, hystrix, indistinctus, mactans, pallidus, renivulvatus, revivensis, tredecimguttatus, variolus

M

Embolus tip/whole embolus

Often/high

No/possible/yes/paternity reduced

Dahl (1902); Smithers (1944); Levi (1959b, 1966); Bhatnagar and Rempel (1962); De Biasi (1962); Abalos and Baez (1963, 1967); Wiehle (1967a); Kaston (1970); Müller (1982, 1985); Levy and Amitai (1983); Breene and Sweet (1985); Andrade and Banta (2002); Berendonck and Greven (2002, 2005); Knoflach and van Harten (2002); Snow et al. (2006); Segoli et al. (2008b); C. Kristensen, personal communication (2008); Neumann (2009)

 

Meotipabituberculata, impatiens

M

Part of embolus

High

Possible

Deeleman-Reinhold (2009) (Thaler memorial)

 

Nesticodesrufipes

A

Male genital tract

High

?

Knoflach (2004)

 

Paidiscurapinicola

A

Male genital tract

High

?

Knoflach (2004)

 

Parasteatodatepidariorum

M

Embolus tip

?/always

Possible

Abalos and Baez (1963); Locket and Luczak (1974); Knoflach (2004)

 

Rhomphaea spp.

A

?

?

?

Gertsch (1979)

 

Simitidionlacuna, simile

A

Male genital tract

High

?

Knoflach (2004)

 

Steatodabipunctata, capensis, castanea, grandis, triangulosa

A

Male bulbal secretions/male oral secretions

High

Not necessarily/yes

Gerhardt (1926); Braun (1956); Levi (1957); Knoflach (2004); Cushing P. personal communication (2008); A. Dippenaar, personal communication (2008)

 

Tidarrenargo, cuneolatum, sisyphoides

M

Pedipalp/whole body

Always

Short term

Knoflach and van Harten (2000, 2001); Knoflach and Benjamin (2003)

 

Theridionadrianopoli, galerum, grancanariense, incanescens, melanostictum, petraeum, pictum, pinastri, refugum, varians

A

Male genitalic and female secretions

Often/high

No/yes

Levi (1959a, b); Gerhardt (1924); Roberts (1993); Knoflach (1997, 1998, 2004)

Theridiosomatidae

Theridiosomagemmosum

A

?

?

?

Roberts (1993); J. Hajer, personal communication (2008)

Thomisidae

Hedanabonneti

M

Embolus and membraneous sheath

?

Unlikely

Chrysanthus (1964); C. Deeleman-Reinhold, personal communication (2008)

 

Mastira spp.

A

Dried sperm

High

 

Lehtinen (2004)

 

Misumenopsbellulus

A

?

?

?

Lehtinen and Marusik (2008)

 

Mecaphesaceler

A

?

High

Possible

Muniappan and Chada (1970)

 

Ozyptilaclaveata

M

Part of pedipalp

High

?

Bertkau (1894)

 

Tharrhalea“simonii”

M

Embolus/membraneous sheath

?

Unlikely

C. Deeleman-Reinhold, personal communication (2008)

 

Thomisusguangxicus

M

Embolus

High

No

D. Court, personal communication (2008)

 

Xysticus spp., lanio

A

?

?

?

Roberts 1993; A. Hänggi, personal communication (2008)

Titanoecidae

Titanoecaamericana

A

?

?

?

M. J. Ramírez, personal communication (2008)

Toxopidae

spp.

A

?

Often

Possible

Forster (1967)

Trochanteriidae

Longrita spp., grasspatch, insidiosa, rastellata

A/M

?

Often

?

Platnick (2002)

 

Platorishflavitarsis

A

?

High

?

Platnick (2002)

Uloboridae

Philoponella spp.

A

?

Often

?

C. Grismado, personal communication (2008)

 

Uloborusferokus

A

Male palpal (and oral?) secretions

High

Possible

Patel and Bradoo (1986)

Zodariidae

Capheriscrassimana, minimus, multipunctatus, obstructus, quinqueguttatus, scharffi, thea, turbatus, waruii

A

?

High

?/possible

Jocqué (1991); R. Jocqué, personal communication (2008)

 

Cicynethus spp.

A

Male cymbial hair glands?

?

Possible

Jocqué (1991)

 

Mallinellavittiventris

A

?

?

?

Jocqué (1991)

 

Neostorena spp.

A

?

Often

?

Jocqué (1991)

 

Platnickia spp., elegans

A

?

?/often

?

Jocqué (1991); Grismado and Platnick (2008)

 

Storenomorpha spp., paguma

A

Male cymbial hair glands?

?

Possible

Jocqué (1991); M. J. Ramírez, personal communication (2008)

 

Tenedos spp.

M

Part of embolus

?

?

Jocqué and Baert (1996)

Zoropsidae

Griswoldiaacaenata

A

?

?

?

M. J. Ramírez, personal communication (2008)

 

Kilyana spp.

M

Base of embolus

?

?

Raven and Stumkat (2005)

 

Krukt spp.

A

?

?

?

Raven and Stumkat (2005)

 

Megateglesbiae

A

?

?

?

Raven and Stumkat (2005)

 

Uliodon spp., cf.frenatus

A

?

High

?

Raven and Stumkat (2003, 2005); M. J. Ramírez, personal communication (2008)

Questionmarks are used when there is no information available. The description of plug frequency is given as rare, often, high according to the anecdotal information given in the papers cited or through personal communications

In this review, we will discuss selected studies that offer valuable insights into the function of the two types of plugs: amorphous mating plugs, and plugs consisting of male genitalia. We have tried to present a complete review of work on mating plugs in spiders, but our presentation will be biased towards more recent studies. A compilation of citations on the family level is given in Table 1. Full information on the species level is accessible on the homepage (http://www.mnf.uni-greifswald.de/fr-biologie/zool-institut-museum/allgemeine-und-systematische-zoologie.html), and we encourage readers to alert us to as yet undetected publications or unpublished findings on the topic.

Terms used

Entelegyne spiders possess an epigynum, a more or less rigidly sclerotized area of the external female genitalia in which the openings of the female “insemination” or “copulatory” ducts are situated (Foelix 1996). The entrances leading to the ducts are called ‘copulatory openings’. The copulatory openings in some species are situated inside a more or less deep depression in the epigynum, called the atrium. In the vast majority of entelegyne spiders the copulatory ducts lead to a sperm storage site from which a fertilization duct connects to the oviduct (through which eggs are laid) (Fig. 1). In some taxa of entelegyne spiders (e.g. Araneidae, Linyphiidae) the anterior part of the epigynum extends caudally as a cylindrical object or in a lip-like manner thereby covering the copulatory openings. Such scapes are often used for genital coupling during mating (Grasshoff 1973; Uhl et al. 2007). Haplogyne spiders generally have the plesiomorphic state of the female genital system, with a single opening that is used for both copulation and oviposition (Fig. 2). Some possess an independently derived sclerotized area also termed “epigynum”.
https://static-content.springer.com/image/art%3A10.1007%2Fs10709-009-9388-5/MediaObjects/10709_2009_9388_Fig2_HTML.gif
Fig. 2

Schematic representation of the female reproductive anatomy of haplogyne and entelegyne spiders. The arrows depict the direction of transmission of sperm into the spermathecae (grey) and out of the spermathecae for fertilization of the eggs (black). Cd Copulatory duct, Go genital opening, Sp spermathecae, Ue: Uterus externus

The copulatory organs in male spiders are the transformed pedipalps (palps) (Foelix 1996). Sperm is transferred from the genital pore to the bulbus genitalis where it is stored until copulation and then released through a structure called the embolus. The embolus is sometimes accompanied by a structure called the conductor that is involved in coupling (Uhl et al. 2007) or is inserted into the female copulatory duct together with the embolus during mating (e.g. Schult and Sellenschlo 1983; Kuntner et al. 2008). The functional unit in the latter case is called embolic conductor.

Mating plugs in spiders

Amorphous/secretory mating plugs

Occurrence and properties

Material that is found on or in the genital opening of mated female spiders is usually amorphous (Fig. 1E–H). Often, it is not restricted to the copulatory openings but covers the epigynum to varying degrees. The epigynal atrium of a fossil female synotaxid spider from the Baltic Amber (Arcometa ?cristata) is completely filled with material (Wunderlich 2004). In some species plugs are so large that they have to be removed in order to identify the species (e.g. Strand 1906; Roberts 1993; Raven and Stumkat 2005; Marusik and Crawford 2006). In other cases, the plug material may only be detected under high magnification (Uhl and Busch 2009). The properties of the materials differ immensely from species to species—it can be flimsy, gelatinous, waxy, sticky, rubbery or extremely hard. In some species the material is so firmly attached to the epigyne that it cannot be removed without damaging the female genitalia (Levi 1957, 1963; Bonaldo and Brescovit 1992; Edwards 1993). Sometimes it is difficult to distinguish between sclerotized projections and actual plug material (e.g. Lehtinen 2004 on Mastira, Thomisidae; L. Lotz, personal communication 2008 on Cheiramiona, Miturgidae) which has led to misclassifications because the material has been considered to be part of the female morphology (Menge 1968; Gertsch 1979). These observations strongly suggest that at least hard plugs, that are difficult to remove by subsequent males evolved as powerful means to secure paternity. Our review of literature indicates that long-term plugs are only known from entelegyne species (Table 1). We expect plugs to be long-term plugs if the material is reported to be hard or if the frequency of plugged females is high. From the female perspective, the application of a hard mating plug compromises sequential cryptic mate choice, but if she accepts a male according to a quality threshold, a plug can help her be sure no other male will be able to introduce sperm. Consequently, females in species with long term plugs are expected to show strong female mate choice before mating in order to avoid costs from mating with low quality males.

However, not all secretions irreversibly plug the genital opening; on the contrary, Jackson (1980) reports that he could easily flip the plug off with an insect pin, and male of the agelenid Agelena limbata were shown to be able to remove plugs which demonstrates that access by subsequent males is possible. Not fully effective plugs are expected on theoretical grounds since 100% effective plugs are not evolutionary stable: They either lead to male avoidance of already mated females and selection on plugs ends or lead to a high selective advantage for males that remove the plugs. Both scenarios result in a partially effective state (Parker 1984).

Mating plugs were also observed in a number of haplogyne pholcid spiders of the genus Belisana (Huber 2005b) but it is unknown whether the material is difficult to remove and long lasting. Latest before or during oviposition the material should be removable in order not to impede oviposition.

Productions sites

Behavioural observations suggest at least three different sites for glands that produce amorphous plug material in the male and one in the female: in the male genital tract (Knoflach 1998, 2004); in the male mouth area (Braun 1956); in the male bulb next to the sperm reservoir (Suhm et al. 1996); and an undetermined site in the female (Knoflach 1998, 2004, Aisenberg and Eberhard 2009). The study by Suhm et al. (1996) of two entelegyne Amaurobius species is the only study to date that clarified the plug production site by ultrastructural methods. They found that the plug material is produced and stored in a gland inside the bulb of the male pedipalp that has no connection to the sperm duct. In Philodromus aureolus (Philodromidae) and Belisana species (Pholcidae) (Huber 1995, 2005b) the material seems to be produced already in the male genital tract since the mass was found to contain secretion and sperm which has led Huber to suggest alternative hypotheses such as protection against sperm desiccation or simply the deposit of superfluous sperm. A fourth possible production site was suggested by Platnick (2000b) who found highly modified setae on the tibial apophysis of male of the genus Paccius (Corinnidae). The setae are bundled and one is elaborated into a scooped-out channel. Epigyneal plugs are frequently found in Paccius females, which led to suggest that the setae play a role in this context (Platnick 2000b).

Female participation in plug production

Interestingly, the material may not be deposited entirely by the male since in some species the plug material is apparently a combination of male and female products. In several entelegyne Theridion species (Theridiidae), plugs seem to be formed by a product from the male genital tract or the male palp as well as a female product (Knoflach 1998, 2004). Plug production occurs during a distinct phase at the end of copulation, and lasts for some minutes up to over an hour (Knoflach 2004). When two Theridion varians males were experimentally prevented from applying secretion from their genital tract to the epigyne (Knoflach 1998) a droplet appeared on the epigyne, but it did not harden and was later absorbed by the female. It remains to be investigated if the droplet is produced by the female as suggested by Knoflach (1998) or if it originates from an additional gland situated in the male palp. In the tetragnathid Leucauge mariana, the female influences the effectiveness of a plug by adding her portion or not (Mendez 2002 cit. in Eberhard 2004; Aisenberg and Eberhard 2009, see “Experimental Evidence on Amorphous Mating Plugs”). These cryptic female decisions can provide efficient means to control the fate of the ejaculate of preferred or unpreferred males and may cause selection on males to produce plug material that circumvents female decisions. Cycles of antagonistic coevolution have been suggested for the plug like `insemination reaction mass’ in Drosophila. The reaction mass that consists of male and female substances diverges rapidly among populations and strongly influences female oviposition and remating behaviour (Knowles and Markow 2001). In order to understand the coevolutionary dynamics of mating plugs investigations on the biochemical aspects involved will be especially revealing.

Experimental evidence on amorphous mating plugs

To date there are five species from as many families in which the adaptive value of amorphous mating plugs has been investigated experimentally: Phidippus johnsoni (Salticidae: Jackson 1980), Agalena limbata (Agelendiae: Masumoto 1993), Nesticoides rufipes (Nesticidae: Molina and Christenson 2008), Oedothorax retusus (Linyphiidae: Uhl and Busch 2009) and Leucauge mariana (Tetragnathidae: Mendez 2002 cit. in Eberhard 2004; Aisenberg and Eberhard 2009). We will discuss these findings in this order.

Phidippus johnsoni (Salticidae)

In the jumping spider Phidippus johnsoni males apply material onto the copulatory openings of the females in 81% of cases (N = 164) (Jackson 1980). The material differs in size, shape, colour and texture. In some cases, one or two discrete plugs are produced that cover one or both copulatory ducts, in other cases a single large mass covers both openings. The material remained on the genital area for at least 2 weeks in 54% of single mated females. However, subsequent males were able to remove a plug in about 70% of cases. Females were checked 24 h after second matings and plugs were either lacking or males had replaced the previous plug. In staged double matings with irradiated first males and non-irradiated second males, Jackson (1980) found that 55% of second males did not sire any offspring, 27% sired all offspring and 18% some of the offspring, suggesting that the material applied functions as a true mating plug that can prevent or impede transfer of sperm by subsequent males. However, these results are tentative since reciprocal mating sequences were not performed and the presence, size and condition of mating plugs were not checked before the second mating trial was staged. Also, copulation duration was extremely variable and its relationship to sperm transfer, plug production, female remating and hatching success remains to be resolved (Austad 1984). The study, however, suggests that first males can at least sometimes succeed in monopolizing paternity of a female`s eggs and that they perhaps achieve this by applying a plug.

Agelena limbata (Agelenidae)

In the agelenid Agelena limbata males can effectively protect paternity by applying secretory material over the genital opening of the female (Masumoto 1993). Males were observed to produce either complete or incomplete plugs. Complete plugs filled the atrium completely and thus covered both copulatory openings that are situated inside the atrium. Incomplete plugs, on the other hand, filled only a portion of the atrium. While complete plugs provided first males with 100% paternity success, incomplete plugs could be removed by rival males, reducing the first male’s share in paternity to 37%. Whether males applied a complete or an incomplete plug, depended on (1) absolute male size, with larger males more likely to produce complete plugs than smaller males, and (2) relative size of male and female (given as the male/female cephalothorax width ratio). In matings with more equally sized mating partners, males were more likely to apply a complete plug. Interestingly, in a later study, Masumoto (1999) found that in A. limbata size assortative mating occurs regularly, with females rejecting relatively smaller courting males with higher probability. Although the reasons for female size-selective mating are unclear, their choice entails a higher probability of receiving a complete plug, which may fully coincide with her interests or not.

Nesticodes rufipes (Theridiidae)

Theridiid spiders produce mating plugs after a long sequence of relatively short insertions with both pedipalps. In between insertions males often leave the female, construct a sperm web and induct additional sperm into their palps (Knoflach 2004). During the last phase of mating, the male transfers a seemingly liquid material into the atrium where the openings to both copulatory ducts are found. Transfer of material may be repeated several times, and the material on the atrium eventually hardens (Knoflach 2004). In the course of a general investigation of female and male mating experience on subsequent reproductive behaviour in Nesticodes rufipes, Molina and Christenson (2008) observed the effect of the presence of a mating plug on the behaviour of both sexes. The presence of a plug was experimentally manipulated by interrupting matings before or after the dabbing behaviour of the male that is associated with the transfer of plug material. Whereas all virgin females were receptive, mated females generally were more aggressive and less receptive. However, females experiencing different treatments differed in the degree of remating: 70% of females that experienced interrupted matings and lacked plugs, but only 20% of females that experienced a complete first mating with plug production remated. As the phases of sperm transfer and plug formation are distinctly separated in this species, the decrease in receptivity already found in plugless females may be due to the transfer of receptivity inhibiting seminal fluids together with sperm which may or may not be in the females’ interest. The few second matings (2 of 10) that occurred with plugged females were found to be incomplete, in that males did not properly anchor their pedipalp and had shorter insertion durations. Since most females allow the transfer of plug material after sperm transfer in unmanipulated matings (Molina 2005, unpublished M.S. thesis, University of Washington), and since plugging results in only partial and possibly ineffective subsequent matings, plugs may successfully secure paternity in this species. This conclusion, however, is tentative, since the sample size for mated females was small and reproductive payoffs from matings with plugged females were not determined (Molina and Christenson 2008). Female contributions to the mating plugs as was suggested or shown for Theridion (Knoflach 1998) and Leucauge (Eberhard and Huber 1998a, Mendez 2006 cited in Eberhard 2004; Aisenberg and Eberhard 2009) were not apparent in this species, but they may have been overlooked (Y. Molina, personal communication 2009).

Oedothorax retusus (Linyphiidae)

Amorphous mating plugs are known from several linyphiid spider species (Table 1) and are probably widespread in the subfamily Erigoninae (dwarf or money spiders) but are difficult to detect due to the spiders’ small size (~2–3 mm body length). In Oedothorax retusus, the material was found only in mated females on one or both copulatory openings, depending on whether a female allowed one or two insertions by the male (Uhl and Busch 2009). Single insertions occurred in 42% of cases (N = 45) and after mating, secretion was never observed in the unused side of the female genitalia. Unmanipulated copulations last 3.5 min on average (N = 68; N. Richter 2006, unpublished Diploma thesis, University of Bonn). Experimental variation of copulation duration showed that the amount of the material was significantly larger after copulations lasting 3 min compared to 1 min (Uhl and Busch 2009), suggesting that plug production is a time related process in this species. In a subsequent experiment, males with one pedipalp (the other was amputated before the trial) were allowed to mate for 1 or 3 min (Uhl and Busch 2009). Second males with one pedipalp were then allowed to mate into either the used or the unused side of the female genital tract. The probability that a second male mated was significantly reduced in the 3-min-used group compared to all other groups. However, copulations into 1-min-used ducts did not differ in duration or in the number of pumping movements from copulations into unused ducts. These findings suggest that the increased amount of secretion after longer insertions in fact functions as a mating barrier for subsequent males. Whether short first matings that are correlated with small plugs nevertheless affect a second male’s paternity if he mates into the used duct is currently investigated. Since female O. retusus ended the first matings in 23% of the cases, and are often aggressive towards males after mating, there is a potential for female mate choice in terms of copulation duration and number of insertions that can have a strong effect on the degree to which paternity of her offspring will be monopolized by a given male. Selective participation in plug production should be investigated since some virgin females (27%) had a small portion of amorphous mass visible inside virgin copulatory ducts that seems to differ from plug material. Interactions between male and female products inside the female ducts as were found for insects (Hosken et al. 2009) are therefore possible.

Leucauge mariana (Tetragnathidae)

The study by Mendez (2002, cited in Eberhard 2004) differs markedly from all other detailed studies available to date in that its focus extends to the female perspective. Mendez demonstrated that copulatory plugs can impede subsequent matings in Leucauge mariana only if the female cooperates in plug production (see also Eberhard and Huber 1998a). First of all, a female that allows a male to mate has several behavioural options to prevent plug production, which occurs at the end of copulation, including kicking the palp away or bending the abdomen in a way that the male can not reach the epigyne. Moreover, females can impede plug formation but permit sperm transfer by not adding liquid to the male’s transferred material. If the female does not add her part, a functional plug cannot be formed. In some cases a flimsy plug was produced only by the female, and experimental removal of such a plug resulted in the appearance of a liquid from the female genital tract that quickly hardened into a flimsy layer. The material alone does not present any significant impediment to subsequent males, only in concert with male products. Originally, the material may have prevented genital infections or sperm desiccation inside the spermathecae. The adaptive value of the female material clearly needs further study. As to the male traits that correlate with female participation in plug production, a recent study by Aisenberg and Eberhard (2009) reveals that specific male copulatory courtship behaviour, i.e. rhythmic pushing on the female’s legs and repeated short insertions with his genitalia are correlated with increased chances that the female will contribute in forming a mating plug. This is the first study that strongly indicates that cryptic female choice is involved in plug production.

Amorphous plugs: Sexual selection and sexual conflict

The investigations presented above demonstrate that amorphous mating plugs play an important role in preventing or reducing sperm competition. These plugs were shown not to be totally effective in preventing the female from remating as is expected on theoretical grounds (Parker 1984).

Variation in plug size was shown to have a strong influence on the likelihood of subsequent insemination. This size variation may result from male body size differences as in Agelena limbata (Masumoto 1993), general male condition, or male mating history (the plug producing gland may be depleted following mating). Ultrastructural investigations of the specific plug reservoir at different time intervals after mating can determine the period needed to refill the reservoir. Data on repeated mating of Oedothorax retusus males, however, demonstrated an only small effect of increased male mating experience on plug size and mating duration (K. Kunz and G. Uhl, unpublished). Males that were mated with three virgin females in succession within 3 h showed high variability in the size of the produced plugs. There was no trend for plug size to decrease with increasing number of matings since even first plugs could be small. Why males of O. retusus, who mostly (77%) terminate copulation, produce small plugs with some females and large plugs with others remains to be investigated. However, males that produced large plugs in their first mating seemed to be slightly depleted of material in their second mating (P = 0.06, N = 11). These data suggest that costs of plug production are not particularly high, but it has not been established yet if producing a plug comes at the cost of reduced sperm production. In insects, correlational evidence suggests important trade-offs among individual products that are transferred during mating (e.g. Moore et al. 2004).

Apart from specific male mating strategies, female traits could affect male remating success and plug efficacy in several ways. First of all, the female genital morphology provides the “rules of the game” for sperm competition as has been argued by Eberhard (1996). If the female genital organization favours sperm from first males, mating plugs will not be effective in altering this sperm priority pattern. On the other hand, female morphology that favours sperm from the last male to mate provides a strong selective advantage for plug production. However, the interaction of female and male morphology will lead to additional variation, depending on whether male genital organs can access female sperm storage sites and remove sperm or not (Uhl 2002).

The morphology of the female epigyne also plays an important role in shaping male opportunities of monopolizing a female. In most spider species and especially in entelegyne spiders, males use their pedipalps in succession: they court, insert e.g. the right palp once or several times and then switch to the left pedipalp, with or without an additional courtship phase. If female copulatory openings are widely separated on the epigynum, a male must achieve two insertions to block both openings with secretion (or parts of his genitalia) and thereby monopolize both female sperm storage sites. This situation offers a high potential for female mate choice: females can allow a male one or two insertions by interrupting mating at different times during the mating sequence. On the other hand, if female genital morphology provides both genital openings close to each other possibly within a single atrium, it is conceivable that males can plug both copulatory openings with a single large mass of secretion from a single insertion. Close vicinity of copulatory openings occurs e.g. in most or at least some Anyphaenidae, Agelenidae, Corinnidae, Lamponidae, Linyphiidae, Oxyopidae, Philodromidae, Salticidae, Sparassidae, Theridiidae, Zodariidae (Table 1), and both openings are often situated in a single atrium which can be filled completely with a single mass. Incomplete versus complete plugs in Masumoto’s study on Agelena limbata (1993), however, do not seem to be the result of mating with one versus two pedipalps, as males invariably used both palps (T. Masumoto, personal communication 2009). Male condition seems to be the main responsible factor for the production of a sufficiently large mass that covers both ducts within the wide genital atrium of the female. The relationships between female genital morphology, insertion mode, plug production and monopolization scheme combined with data on reproductive success need to be explored in more detail in order to reveal male and female reproductive strategies and constraints.

Females are further expected to influence the production and fate of mating plugs behaviourally. Females can physically prevent or impede plug deposition, especially in species in which plug production occurs at the end of mating in a separate induction phase as in some Amauribiids and Theridiids (Table 1). In several theridiids, males leave the female after several phases of sperm transfer, produce a sperm web, add substance to the web from the genital tract, take up the substance in the pedipalps and then transfer the substance onto the female genital area. This substance then hardens and represents the mating plug (Knoflach 2004). It is not yet clear whether females sometimes prevent the males from adding the plug. Further, if a plugged female remains receptive, she may or may not provide a subsequent male with sufficient time to remove the plug depending on his performance during courtship and the initial mating phase. Removal of plugs sometimes requires a substantial proportion of the duration of the second male’s copulation in Phiddipus johnsoni (Jackson 1980) and Leucauge mariana (Mendez 2002, cited in Eberhard 2004). Finally, a female may add a substance that is required for plug efficacy or not—as in Leucauge mariana (Mendez 2002, cited in Eberhard 2004; Aisenberg and Eberhard 2009). If polyandry is advantageous to females, we expect a selective advantage for cryptic female abilities to manipulate the production, application and fate of the plug (Eberhard 1996; Hosken and Stockley 2004; Hosken et al. 2009).

On the other hand, being plugged may also be advantageous for females e.g. if plugs reduce disturbance by other males. In fact, mated females are often aggressive or less receptive but this may not be due to the plug itself but to substances that are transferred along with the male ejaculate (Chapman and Davies 2004). Preventing a male from plug application resulted in higher aggression and reduced receptivity in females of a theridiid spider, which suggests that the plug material is not responsible for these changes in female receptivity (Knoflach 2004). Clearly, from a male perspective, there is a high selective advantage from transferring manipulative agents early during mating instead of running the risk of being refused to leave a plug. In species with continuous plug production as seems to be the case in Oedothorax retusus, these types of agents may be found in the plug material as well as in the seminal secretion. To date, no research is available in spiders on the possible hormone-like action of male seminal substances although it is obvious from recent studies that there is a high diversity of seminal secretions in spiders (Michalik and Uhl 2005; Michalik 2009).

Mating plugs formed by male body parts

Types of plugs: parts of genitalia, whole palps and whole males

Plugs constituted by broken pieces of the male’s own genitalia inside the female are surprisingly common in spiders (Fig. 1A–D). Taxonomists who routinely dissect out and clear internal female genitalia often find pieces of male genitalia particularly in species of the families Araneidae, Nephilidae and Theridiidae; in some of these sexual cannibalism occurs, but in others it is not known (Table 1). Usually the parts found inside the female copulatory openings, copulatory ducts or even spermathecae are the broken-off pieces of the male sperm transferring structure, the embolus. In araneid species in which males possess a so-called embolus cap (embolic cap), this specialized distal tip of the embolus is left in the female after mating. In the araneid Argiope species, the pieces can vary from a large part of the embolus to an almost unnoticeably small tip, even within a single species (Uhl et al. 2007). In some Nephilids (Nephila, Herennia, Nephylengys), males either leave part of the long, rod-like embolus behind or a combination of embolus and part of the conductor (embolic conductor) (Kuntner et al. 2008). In Theridiids it is also generally a part of the rod-like embolus that is left behind (Table 1). In some oxyopid spiders, on the other hand, males leave the apex of the paracymbium, a structure of the pedipalp that is not involved in sperm transfer but is very likely important in genital coupling (Table 1). Surprisingly, the available taxonomic literature even offers information on genital mutilation in some species of haplogyne mygalomorph spiders. In several species of the genus Neocteniza (Goloboff 1987), emboli were found stuck in one or both ducts each leading to a spermatheca. Since more than one embolus per duct was rarely found, female remating probability seems to be restricted. Due to the haplogyne female genitalia the plugs in Neocteniza will need to be dislodged prior to oviposition otherwise sperm cannot be released from the spermathecae to meet the eggs.

In some species the male leaves the whole pedipalp behind. In the Theridiid ‘one-palp’-genus Tidarren (Knoflach 2002), males invariably amputate one of their pedipalps after the final moult, which leaves them with only one palp to reproduce. During copulation the female of T. argo emasculates the male, i.e. she separates him from his sole pedipalp. She then feeds on his corpse while the palp remains attached to the female’s epigyne for about 4 h and seems to continue to transfer sperm in this detached state (Knoflach and van Harten 2001). Females mate more than once in this species, so it is possible that subsequent males have a share in paternity, and the detached palp may thus serve to reduce the likelihood of subsequent inseminations. Similar findings are available for the theridiid Echinotheridion gibberosum in which males also amputate one of the pedipalps before mating, and are emasculated during copulation (Knoflach 2002). In Tidarren sisyphoides, Knoflach and Benjamin (2003) found that after the onset of copulation males die spontaneously and remain on the female’s epigynum for some minutes or hours before they are removed by the female without being cannibalized. In Tidarren cuneolatum, males also die during mating but are eventually cannibalized (Knoflach and van Harten 2000). Whether the male’s palp or the male soma reduce the probability of remating by the females, and the reasons for the highly variable attachment times in these species remain to be explored.

Male death and short term mating plugs have been investigated in more detail in Argiope aurantia (Foellmer and Fairbairn 2003; see also Sasaki and Iwahashi 1995 for A. aemula). In A. aurantia, males invariably die a programmed death while the second pedipalp is inserted. A physiological process commences within seconds after the onset of the second insertion that leads to cessation of the male’s heartbeat (Foellmer and Fairbairn 2003). Dead males are firmly attached to the female by means of their still inflated pedipalp, thus serving as a whole body mating plug. The effect of male sacrifice depends on whether the male mates with a mature and often aggressive female or with a freshly moulted female that cannot attack the male. In matings with mature females, attachment times are only 8 s on average since dead males are quickly removed by the females, whereas in matings with freshly moulted females dead males remain attached to the female for 15–25 min before they are removed. During this phase, the corpses function as whole body mating plugs since they often prevent rival males from copulating. Despite the benefits of mating with defenceless females, such opportunistic matings occur in only 60% of cases (Foellmer unpublished in Foellmer and Fairbairn 2003). Possibly, there are as yet undetected costs of mating with freshly moulted females that pertain to sperm storage and sperm utilization. Irrespective of the different mating tactics, it seems that the benefits of dying during mating outweigh the costs of losing all further mating opportunities in A. aurantia (see “Assessment of Future Mating Opportunities of Damaged Males”).

Experimental evidence on genital damage

Although numerous descriptive studies exist that illustrate the occurrence of genital damage and depict female genitalia with broken off male genital parts inside the copulatory ducts or spermathecae (Table 1), few studies have investigated the adaptive significance of male mutilation. We will present and discuss information available on the three most intensively studied genera, Latrodectus (Theridiidae), Argiope (Araneidae) and Nephila (Nephilidae).

Widow spiders: Latrodectus

In many species of the theridiid spider genus Latrodectus, the tip of the embolus breaks off at a weak point, and remains inside the female genitalia (Wiehle 1960; Uhl 2002; Berendonck 2003). The broken pieces do not necessarily prevent the female from remating since more than one piece can be found in the duct leading to a given spermatheca or in the spermatheca itself (see Refs. in Table 1). However, in several species only a single tip was found in each spermathecal entrance, whereas several more could be found in the duct leading to the spermathecae but the order of deposition is not known (Uhl 2002). A morphological examination of the female genitalia of Latrodectus revivensis demonstrated that an embolus tip can close the narrow entrance to the spermatheca very tightly, which suggests that a male who succeeds in placing his embolus tip correctly can monopolize the sperm storage site (Berendonck and Greven 2002). In fact, a paternity study including post-copulation dissections of females on L. hasselti showed that males have lower paternity if they deposit the embolus piece in sub-optimal locations (Snow et al. 2006), which suggests that copulatory organ breakage allows males to avoid sperm competition. However, female cannibalistic behaviour also seems to play an important role in the deposition of the embolus tip. As Snow et al. (2006) suggested, investigations of male and female effects on plug deposition and retention are required to understand the coevolutionary dynamics involved.

Wasp spiders, St Andrews cross spiders: Argiope

A further example for detached genital parts that can reduce sperm transfer comes from the orb-weaving spider Argiope bruennichi (Nessler et al. 2007a). Males of A. bruennichi damage their genitalia at two predetermined breaking points, and the type of damage differs between populations (Uhl et al. 2007). In this species, sperm transfer is positively correlated with copulation duration (Schneider et al. 2006). Embolic parts are left behind in the female`s insemination duct in about 80% of matings, and they significantly reduced copulation duration and paternity of rival males that inserted their palp into the same duct (Nessler et al. 2007a; Schneider and Lesmono 2009). If males used the opposite (unused) duct, copulation duration was much longer than matings with virgin females, suggesting that males assess the mating status of the female and adjust their copulation duration accordingly, as occurs in many other arthropods (Simmons 2001). Interestingly, genital mutilation occurred not only in matings in which the male was cannibalized, but likewise in matings in which the male escaped from the female. Thus, a functional association between sexual cannibalism and genital damage as suggested by (Miller 2007) has not been found. We concluded that genital damage in this species is not a counteradaptation to sexual cannibalism, but primarily an adaptation against sperm competition (Nessler et al. 2007a). Female effects on the position and retention of a plug have not been explored yet.

In the congener A. lobata, there is a strong relationship between sexual cannibalism and genital damage (Nessler et al. 2009). Cannibalized males damaged their pedipalps in 74% of cases whereas genital damage occurred only in 15% of matings in which males escaped from the female. Interestingly, sexual cannibalism is less frequent in this species (60%) and the overall plugging rate is especially low (14%); but when plugging occurred, paternity of a subsequent male who used the same duct was extremely low (1%). The results suggest that besides sperm competition, cryptic mate choice mechanisms may be at work. Females are in control of sexual cannibalism and they might choose superior males to plug her genital opening. Whether a female cannibalizes a given male does not seem to depend on the male’s size and weight (Nessler et al. 2009), however, but other male traits have not yet been studied.

In sexually cannibalistic species males should be selected to distinguish between plugged and unplugged genital openings if the risk that they are cannibalized during their first insertion is high and especially if using a plugged duct results in reduced paternity. Two experimental studies showed that males avoid using an already plugged genital opening. Foellmer (2008) found for Argiope aurantia that second males use the unused insemination duct in 72% of cases. A large piece of the embolus broke off in 94% of cases, and it seems plausible that the broken-off genital tips can be detected and favour discriminative male abilities. Since the male palpal bulb lacks neurons (Eberhard and Huber 1998b) we expect a sense organ on the cymbium, a structure at the base of the palp. Whether the 28% of males that used a plugged opening sired any offspring was not investigated.

Golden silk spiders: Nephila, Herennia

Within the Nephilidae, male genital damage seems to be widespread in Nephila, Nephilengyns and Herennia (see Table 1) and is treated as an autapomorphy for this group by Kuntner et al. (2009b). Experimental and detailed descriptive data are only available for the genus Nephila, so we will restrict our focus to this group. In the golden orb-weaver Nephilafenestrata males usually (96%) break the tip of both the conductor and the embolus during copulation, and these parts remain inside or protrude slightly from the female copulatory ducts (Fromhage and Schneider 2006). Since these genital fragments prevented insertions of second males, and paternity success was shown to be determined by the relative number of insertions performed by the first and second male (Fromhage and Schneider 2005a) genital parts indeed can be considered to function as mating plugs. However, like in Argiope aurantia, some second males succeeded in using a plugged genital opening. Second males can successfully mate into a plugged genital opening if they have enough time and are not disturbed by another male. Males that have both embolic conductors broken are functionally sterile, but often survive in this species and vigorously defend the female against rival males (Fromhage and Schneider 2005b).

In N. plumipes, the tip of the embolic conductor also typically breaks off during mating, but the risk of sexual cannibalism is high for mating males (Schneider and Elgar 2002). Contrary to N. fenestrata, fragments of the male palp in the female genitalia did not prevent females from re-mating, and males who copulated transferred similar amounts of sperm into used and unused ducts (Schneider et al. 2008) and first and second males sired similar numbers of offspring (Schneider et al. 2001). Paternity share in this species is correlated with the duration of copulation (Schneider and Elgar 2001). Genital damage in N. plumipes may be a side effect of a male adaptation to achieve long copulations. Male genital structures in N. plumipes and especially the curved ending of the conductor together with a triangular process at its tip may have evolved as holdfast devices to remain attached to the female’s copulatory organ despite her attack. Males stay in copula even when the females attempt to dislodge them, wrap them with silk and bite them (Schneider and Elgar 2001; Schneider et al. 2001). Eventually the embolic conductor snaps and remains inside the copulatory opening. Whereas males may profit from long copulations and happen to loose their genital tips during the attempt to stay attached as long as possible, females may test the efficacy of male coupling. To what extend male coupling efficacy is heritable remains to be investigated.

In Nephila inaurata madagascariensis males had shorter copulation durations when they copulated in a previously used copulatory opening (Schneider et al. 2005a, b). The authors assume that copulation duration is positively related to sperm transfer and/or paternity as was found for the congeners N. plumipes and N. edulis (Schneider et al. 2000; Schneider and Elgar 2001). Whether the observed negative effect on copulation duration was due to stuck parts from the previous male is uncertain since broken off embolus tips were found in the genital tract of only 18% of 11 females that were dissected after mating (Schneider et al. 2005b). Female choice, limited sperm storage capacity or a plug effect all offer possible explanations for this correlation. If copulation duration is correlated with paternity success, second males are expected to be able to discriminate between previously used and unused genital tracts. Interestingly, second males were not more likely to copulate with either of the two types of ducts. Nevertheless, if they mated into unused ducts copulation duration was longer compared to copulation durations of virgin females. This demonstrates that males may have some means of detecting the mating status of the female. However, since sexual cannibalism is infrequent in this species (10%), the selective advantage of discrimination abilities may not be as pronounced as in other Nephila species. The low degree of sexual cannibalism is probably related to the fact that the onset of male courtship and mating requires that the female be feeding on a prey item, as occurred in 91% of the copulations observed (Schneider et al. 2005a, b). The male strategy of waiting until the female is feeding is known in several Nephila species in which sexual cannibalism occurs (Robinson and Robinson 1980).

The first indication of male mate choice in a species with genital damage comes from the nephilid Herennia multipuncta. Parts of the male genitalia were more likely to be found in the female genital tract in matings with large females (Kuntner et al. 2008). This seems to suggest that males prefer large, fecund females but it could also mean that large females break off male palps more effectively. In Herennia, males that escape female cannibalism and whose palps are damaged break off their palpal bulbs, and physically defend the female from remating as emasculated males. Since the removal of the palp in the one-palp spider Tidarren sisyphoides was found to greatly increase locomotor performance (Ramos et al. 2004), emasculation may render Herennia males more agile during post-mating encounters with rival males.

Assessment of future mating opportunities of damaged males

Being cannibalized by the female should not be in a male’s interest unless benefits he derives are so high that they override the costs of loosing further mating opportunities. Male genital mutilation is generally assumed to be advantageous for males due to the low probability that the male will live to encounter another female and the high mortality risk for males during mate search (Andrade 2003; Snow et al. 2006). However, strong male competition is required to select for high cost paternity protection and have been shown to favour male monogamy in a theoretical model (Fromhage et al. 2005, 2008). Since high mate search mortality effectively reduces male competition, a strong male biased tertiary sex ratio is necessary to maintain competition (Fromhage et al. 2005, 2008).

Morphological data demonstrate that males are adapted to monogamy. Males of the theridiid Tidarren argo stop spermiogenesis when they reach adulthood and their testes atrophy (Michalik et al. 2009). Sperm production also stops after male maturation in various Nephila and Argiope species with high sexual cannibalism (P. Michalik, personal communication) and used pedipalps are not recharged in Argiope (Herberstein et al. 2005). As a consequence, male sterility seems to be primarily a matter of sperm depletion not of mechanical difficulties caused by male genital damage.

However, even if the pedipalps are charged only once and sperm production stops thereafter, the ejaculate stored within the palpal bulb could be strategically allocated to several mating partners in species with a relatively high male survival rate. In this case, male fertility might be reduced by damage to his genitalia. In fact, a study on Latrodectus pallidus, a widow spider with low probability of sexual cannibalism showed that 10% of males succeed in successfully inseminating two females despite a high probability of genital damage during the first mating (Segoli et al. 2008a; see Breene and Sweet 1985 for L. mactans). Whether males of this species produce sperm for a longer time period and thus are able recharge their pedipalps, or use only a certain amount of the sperm in the pedipalp for each mating, or use only one palp per mating is as yet unknown.

Species with high male survival probability may follow a different reproductive strategy compared to the species with a high probability of sexual cannibalism. However, genital mutilation itself does not seem to lead to functional sterility even in the highly cannibalistic L. hasselti males (Snow et al. 2006). When embolus tips were cut experimentally from virgin males, they were still able to inseminate females, had similar copulation durations and transferred similar amounts of sperm compared to males with intact emboli (Snow et al. 2006). This study demonstrates that males are potentially able to mate multiply (e.g. Foellmer 2008).

Sexual selection and sexual conflict

In species in which males leave body parts behind as mating plugs, the costs to the males strongly depend on the consequences of the damage for their reproductive future and the benefits naturally depend on the efficiency with which rivals will be excluded. Genital damage in concert with sexual cannibalism can limit males to extremely low mating rates. Indeed, it seems that most species with genital mutilation show a male biased effective sex ratio and a fierce competition for virgin females (Robinson and Robinson 1980; Robinson 1982; Miller 2007). The male biased sex ratio may follow from a strong sexual size dimorphism which is caused by longer female maturation times compared to males. Under such conditions, more males than females may get to mate and a monogynous mating system can evolve as was demonstrated in a mathematical model by Fromhage et al. (2005). A monogamous male will be selected to allocate his maximal effort into a single female.

In order to monopolize a female, the male has to leave effective obstructions in both female sperm storage organs. This requires two insertions that in some species are interrupted by an additional courtship bout. The separation of insemination of both spermathecae provides the female an option to control monopolization by a certain male by selectively allowing a second insertion or not.

Using genital plugs does not allow plugging both copulatory openings with a single insertion, whereas a large enough mass of secretion may cover both openings. The alternative strategy to monopolizing a single female could be to try to mate with two females in succession but use only a single palp during each mating event (bigyny). Both scenarios were recently modelled by Fromhage et al. (2008) who found that the strategies theoretically can coexist as alternative mating strategies under negative frequency dependent selection.

Clearly, male–male competition will not only favour defence mechanisms but also offensive traits that overcome defences (Parker 1984) and there is evidence in a few species that males can remove or bypass plugs applied by previous males (above, Schneider et al. 2008; Kuntner et al. 2009a). Nevertheless, effectiveness of genital damage as plugs should be expected to be higher compared to the effectiveness of a secretory plug since the costs of using genital plugs are likely much higher. A high effectiveness in genital plugging will result in a strong selective advantage for being the first male to encounter a freshly matured female or a penultimate female nymph. Indeed, the “suitor phenomenon” is common in Argiope, Nephila and Nephilengys, most of which show some degree of genital damage (Robinson and Robinson 1980; Miller 2007). In many other spider species, the mating tactic of cohabitation, in which the males remain with juvenile females until they mature, are common (Jackson 1986). This suggests that males profit from mating with virgin females, possibly partly because of plug production.

The deposition of a permanent genital plug is costly for the female if she benefits from multiple mating (reviewed in Eberhard 1996; Simmons 2001; Arnqvist and Rowe 2005; see also Uhl et al. 2005 for a spider). Under such a situation, females are expected to evolve countermeasures that prevent male monopolization. “Premature” sexual cannibalism, such as killing a male after his first insertion could be such a strategy. The female would secure a sufficient sperm supply by permitting one insertion and would leave one spermatheca for a second male. Storing ejaculates from different males in two separate spermathecae opens up possibilities for cryptic female choice (Eberhard 1996; Hellriegel and Ward 1998), as suggested in an experimental study on A. bruennichi (Schneider and Lesmono 2009) and A. lobata (Welke and Schneider 2009). Moreover, females may have means to prevent plugging or to remove the plug, as was observed in two Argiope species in which females removed plugs by cleaning themselves (G. Uhl, personal observation; Strauss et al., unpublished). One the other hand, females can test the complex coupling and plugging capabilities of males by attacking early and attempting to remove the plug. A precisely deposited plug that “survives” this test may be used as an indicator of male quality. Whether and to what extent male coupling and plugging abilities are heritable and whether they are correlated with other male traits promise to be important aspects of future research.

Combining amorphous material and male genital parts

It has long been known that there is an interesting combination of amorphous material and male genital damage in the oxyopid spider Peucetia viridans (Brady 1964 and Refs. in Table 1), although these additional parts had been described earlier as part of the epigynum by Petrunkevitch (1930). Brady (1964) described that each of the two copulatory openings situated in a funnel-shaped atrium were usually plugged with a hard, black material and that the distal portion of the paracymbium of the male palp often protruded from this material. He suggested that plugging of the female duct should prevent remating of both females and males of the given mating pair. Ramírez et al., unpublished performed a detailed investigation on male remating probability, the degree of male mutilation, and amorphous plug production. Males that were allowed to mate with three different females successfully inseminated several females in succession. The loss of the tip of the paracymbium did not render the male functionally sterile. The probability that the paracymbial processes ended up in the female tract was high in the laboratory but only in about 50% of cases was it accompanied by amorphous material. This demonstrates (1) that the amorphous matter does not result from breakage of the male genitalia and leakage of male haemolymph and (2) that the process can remain in the female without being anchored in amorphous matter. Further, the size of the mass differed. Some filled the atrium and blocked the copulatory ducts; others only partially filled the atrium, and did not block the ducts. Such size differences may have significant consequences for female remating probability and plug removal by a rival male. The study raises the question of whether the breakage of a part of the male genital organ reduces male vitality and competitiveness in sperm competition and to what extent plug efficacy depends on the presence of the paracymbial process, secretion or both.

Further examination of females collected at four different field sites at the same time of the year demonstrated that the presence of the male process as well as the presence and state of the secretion varies between populations. In one population, none of the nine adult females investigated had secretion or a paracymbial process. In another population processes were found in one or both openings in 38% of the females, and one or two complete portions of secretion were found in 59% of cases (N = 34). Since plugs were less common in a population from a more humid coastal site, the authors suggest reconsidering the desiccation hypothesis for mating plugs.

Male genital damage to the apex of the paracymbium seems to occur also in other Peucetia species (P. flava, P. macroglossa: Santos and Brescovit 2003; A. J. Santos, personal communication 2008), but it is not known to what extent the genital parts are combined with secretion. The type of genital mutilation is an informative character for phylogenetic studies, since males of Tapilinus longipes are also known to mutilate their paracymbium (A. J. Santos, personal communication 2008), whereas males of Schaenicoscelis leucochlora mutilate the apex of their conductor (A. J. Santos, personal communication 2008) (Table 1).

The nephilid spider Nephila pilipes (N. maculata of Robinson 1982) shows genital mutilation in about 50% of the case observed (Kuntner et al. 2009a). Plugging in this species seems to be non-functional in terms of monopolizing a female since multiple plugs can be found in a single insemination duct. Plugs can consist of thin tips of the embolus or short pieces of emboli and the surrounding conductor. In addition, in some females the epigynum was completely covered with a hard amorphous matter in which numerous embolus parts could be embedded. The producer and the function of the plugs are as yet unknown.

In future studies on male mutilation in Nephila and Argiope the presence and frequency of amorphous matter should be considered more carefully, since several species may use secretions to complement male genital damage (personal observation by the authors). Whether the substance is produced by the male or the female, or whether it is a combination of secretion from both sexes, as seems to be the case in some theridiid spiders (Knoflach 2004), is crucial for evolutionary interpretations. In addition, the composition of secretions and the potential physiologically active components need to be studied to see whether male components manipulate female receptivity and reproductive physiology as has been shown for many insects (Chapman and Davies 2004). Although plugs in spiders likely evolved as measures to prevent future copulations of rivals (Simmons 2001), whether plugs retain their effectiveness will strongly depend on the interests of both sexes. By adding or not adding components to the secretion, females may be able to circumvent male monopolization and may have a means to selectively favour reproductive success of specific males.

Conclusions and outlook

As expected from the specific sexual morphology of haplogyne and entelegyne spiders mating plugs predominantly occur in Entelegynae which typically possess separate openings for insemination and oviposition in females (Table 1). Mating plugs can consist of secretion or parts of the male genitalia. For some species of entelegyne spiders plugs have been shown to serve as paternity protection devices, with different degrees of effectiveness between species. However, alternative functions such as preventing sperm desiccation or passive sperm loss may be side effects or even primary functions of mating plugs. Moreover, secretions may contain substances with cryptic effects on female physiology and behaviour that favour the male`s reproduction, similar to what is known for accessory seminal proteins in insects (Eberhard and Cordero 1995; Arnqvist and Rowe 2005). Whether these alternative functions apply for spider mating plugs cannot be assessed at this state.

While secretory plugs likely come at a relatively low cost for the male, the plugs composed of his own genital parts may severely compromise future use of the mating organ and thereby limit mating rate. Genital mutilation co-occurs with other factors such as sexual cannibalism in some species that are associated with monogynous mating systems and terminal investment in a single mating partner. Future research should determine whether there is a causal connection between cannibalism and genital mutilation, and specifically whether genital damage is a consequence of sexual cannibalism or vice versa. Moreover, we need to clarify whether genital mutilation evolved independently of secretory mating plugs or as a replacement or addition to a possibly less effective way of plugging. Especially the genus Peucetia lends itself to study this question since amorphous plugs, broken-off genitalia as well as a combination of both can occur.

The present state of information (Table 1) implies that secretory plugs are more common than mutilated genitalia. There are several entelegyne families that are particularly prominent in our review: Araneidae, Nephilidae and the Theridiidae. It is unclear whether these families are indeed special or whether they are simply better studied than other families. It is important to note that the table only contains positive evidence, i.e. reports of the presence of mating plugs; there are no data about species which definitely lack plugs and many species may exist for which plugs were not considered important enough to be mentioned. It is crucial to collect comprehensive data for all spider families from museum collections in order to elucidate the distribution of mating plugs in spiders further.

In order to address evolutionary questions and to develop well founded predictions concerning the adaptive value of plugging, more experimental studies are needed. The selective advantage of plugging should preferentially be investigated in species in which plugging can be prevented without disturbing normal mating behaviour. This is the case in some theridiids (Knoflach 1998) that lend themselves to detailed experimental studies on the various possible effects of secretory plugs because the plug is produced following insemination. Similarly, selected araneids and nephilids are ideal to study the causes and consequences of genital damage since the species differ in the probability of genital damage and sexual cannibalism. Once phylogenetic studies are available that can be combined with detailed investigations on plugging effects, the frequency of sexual cannibalism, and information on the species’ ecology (see Miller 2007), we will be better able to interpret the evolution of genital damage. Experimental manipulation of one of the paired genitalia of entelegyne spiders, or of the particular parts of the male genitalia that form the plug offer exiting and powerful approaches (Eberhard 2004; Snow et al. 2006; Nessler et al. 2007b). Studies that identify the interests of females and the ways in which females can influence plugging efficiency and male paternity success are also highly needed. They may reveal complex interactions between the sexes and possibly reproductive coevolution on the biochemical level that evolved in the context of mate choice or sexual conflict.

Acknowledgments

We thank many colleagues for alerting us to relevant publications or contributing to the unpublished information compiled in Table 1: Gerd Alberti, Tharina Bird, Angelo Bolzern, Robert Bosmans, Antonio Brescovit, Charles Christensen, David Court, Paula Cushing, Christa Deeleman, Ansie Dippenaar, Jason Dunlop, Janet Edmunds, Matthias Foellmer, Volker Framenau, Cristian Grismado, Ambros Haenggi, Jaomir Hajer, Mariella Herberstein, Gustavo Hormiga, Bernhard Huber, Robert Jackson, Peter Jäger, Rudy Jocqué, Barbara Knoflach, Martin Kreuels, Torbjörn Kronestedt, Matjaz Kuntner, Katrin Kunz, Pekka Lehtinen, Herbert Levi, Leon Lotz, Jean-Pierre Maelfait, Yuri Marusik, Yamile Molina, Christoph Muster, Norman Platnick, Jerzy Prószynski, Martín G. Ramírez, Martín J. Ramírez, Robert Raven, Linda Rayor, Adalberto Santos, Nikolaj Scharff, Martin Schmidt, Csaba Scinetar, Michal Segoli, Diana Silva-Davila, Helen Smith, Peter van Helsdingen, and Jörg Wunderlich. Peter Michalik kindly designed Fig. 1. This work was supported by the German Research Council (DFG Uh/87-5-1) and a Maria von Linden fellowship of the University of Bonn to GU which is gratefully acknowledged. This paper is dedicated to Bill Eberhard.

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© Springer Science+Business Media B.V. 2009