Table Of Content1999. The Journal ofArachnology 27:135-141
SEXUAL SELECTION IN PHOLCID SPIDERS
(ARANEAE, PHOLCIDAE):
ARTFUL CHELICERAE AND FORCEFUL GENITALIA
Bernhard A. Huber: Department of Entomology, American Museum of Natural
History, Central Park West at 79th Street, New York, New York 10024 USA
ABSTRACT. Two aspects of pholcid reproductive biology are reviewed and appear best explained by
sexual selection by female choice: the rapid and divergent evolution of male chelicerae (and clypei in
some groups) which contact the female epigynum during copulation and probably act as copulatory court-
ship devices; and the often exceptionally strong pedipalps in males, which possibly function in correlation
with the ‘valve’ in the internal female genitalia.
The last decades have seen a promising in- particular aspects: on non-genitalic contact
crease of studies examining spider reproduc- structures which appear to evolve under se-
tion from an evolutionary perspective (review: lection similar to that acting on genitalia, and
Elgar 1998). In most cases, the mechanisms on the unusual phenomenon of copulatory
of sexual selection in spiders are much the courtship associated with vigor.
same as those documented in insects andother Voucher specimens of all unnamed species
major groups (see e.g., Eberhard 1996, where are deposited at the American Museum of
almost every spider example used to docu- Natural History, New York, and labeled with
ment a specific mechanism of cryptic female an I.D. number (“B.A.H. 1999 I.D.# 1-6”)-
choice is accompanied by at least one insect
ARTFUL CHELICERAE
or mammal example). Some details, however,
make spiders either especially useful (e.g., the Pholcids are not unique in having species-
pairedness of genitalia for studies of fluctu- specific copulatory contact structures (Eber-
ating asymmetry - Huber 1996b), or especial- hard 1985). However, pholcids are unique, at
ly interesting (e.g., the apparent lack of both least among spiders, with respect to the wide
muscles and nerves in the male intromittent range of non-intromittent male structures that
genitalia - Eberhard & Huber 1998). (For fur- are sexually modified (practically the entire
ther, though less unique, spidercharacteristics, palp is sexually dimorphic in most pholcids,
see Elgar 1998.) including coxa and trochanter). Two male
In the present paper I will briefly review structures deserve special attention: the che-
some recent advances in one particular spider licerae and the clypeus. At least one of them
family, the pholcids. Pholcids are the only contacts the female during copulation in all
non-entelegyne spiders whose reproductive species studied (Huber 1994, 1995, 1997b,
biology has been carefully studied in several 1998b; Huber & Eberhard 1997; Uhl et al.
&
species (Eberhard 1992; Eberhard Briceno 1995), and the chelicerae in particular are of-
1983, 1985; Huber 1994, 1995, 1996a, b, ten the most species-specific and taxonomi-
1997a, b, 1998a, b, c; Huber & Eberhard cally useful structures. Modifications range
&
1997; Raster Jakob 1997; Uhl 1993, 1994; from hairs ofdifferent shapes to cones, round-
Uhl et al. 1995; Yoward 1998). Further ad- ed, pointed, hooked and blade-shaped apoph-
vantages for the study of sexual selection are yses, and even to sexually dimorphic fangs
the number of synanthropic species that are (Figs. 1-4, 10, 11, 13, 14). Several hypotheses
available worldwide and readily maintainedin might explain this phenomenon: (1) reproduc-
the laboratory forin depth single-species stud- tive isolation hypotheses (lock-and-key and
ies, and a rich and diverse (mainly tropical) genitalic recognition - reviewed in Eberhard
fauna for comparative studies. 1985); (2) the “conflict of interest hypothe-
For reasons of space, I will focus on two sis” (Alexander et al. 1997); (3) sexual selec-
135
136 THE JOURNAL OF ARACHNOLOGY
—
Figures 1-7. Sexually dimorphic structures in male pholcids, SEM. 1. Cheliceral apophyses in Uthina
sp. (I.D. #1); 2. Modified hairs on the chelicerae ofModisimus dominical Huber; 3. Modified hairs on the
chelicerae of Spermophora senoculata (Duges); 4. Sclerotized cones on the chelicerae of Physocyclus
guanacaste Huber; 5-6. Eye turret ofModisimus culicinus (Simon), in lateral and frontal view, showing
frontal lobe; 7. Femur of Modisimus tortuguero Huber, showing a spine, a “normal” tactile sensillum,
and several almost perpendicular hairs that cover the femora of only male walking legs. Scale bars: 0.01
mm mm mm
(1-3); 0.05 (4, 7); 0.1 (5, 6).
HUBER—SEXUAL SELECTION IN PHOLCID SPIDERS 137
tion by male-male competition (Eberhard & epigynum also carries a large apophysis on
Bricefio 1985); (4) the “sperm holder hypoth- each side ofthe hood (Figs. 8, 9), so that only
esis” (Brignoli 1973); (5) sexual selection by males with exceedingly long cheliceral apoph-
female choice (Eberhard 1985, 1996). yses can reach the hood (Figs. 10, 11). Thus,
Reproductive isolation hypotheses assume “genitalic arms races” ofthis sort may reflect
that species-specific differences in pholcid selective female cooperation (the female pro-
chelicerae evolved because they prevent hy- vides ahood for those males able to overcome
bridization. The lock-and-key version does her obstructive apophyses) rather than female
this on a mechanical level, the genitalic rec- resistance to coercive males. Revealingly, the
ognition hypothesis on a sensory level. Both females of several putative close relatives
seem unlikely to account for the phenomenon have the cooperative structure (the hood) but
in a general way. Often there is no female not the barrier (the apophyses) (Fig. 12). Ac-
“lock”, for instance in most Modisimus spe- cordingly, their males’ cheliceral apophyses
cies where the epigynum against which the are rather inconspicuous (Fig. 13), but nev-
male chelicerae are pressed during copulation ertheless species-specific in form.
is just a flat plate, but the chelicerae are nev- Male-male competition is equally unlikely
ertheless species-specific (Huber 1998a). Even to provide a general explanation (Huber
in cases with a lock-and-key like fit, the hy- 1994). In most species the modifications seem
pothesis that such fit evolved to avoid cross- highly inefficientforcombat, and in some cas-
specific pairings is dubious because natural es where their shape might suggest such a
selection should favor early species recogni- function (as in the Ecuadorian pholcid illus-
tion (Eberhard 1985, and references therein). trated in Fig. 14; I.D. #3) the female mor-
However, transitory selection on cheliceral phology strongly indicates their use during
morphology in a species-isolationcontextcan- copulation (the epigynum is unusually broad
notberuled out, andmay have beenimportant and at the lateral extremes provides two blind-
in the past (Shapiro & Porter 1989). ended cuticular tubes, whose location and
The “conflict of interest hypothesis” (Al- spacing indicates that they are used to accom-
exander et al. 1997), applied to pholcid che- modate the male fang-apophyses: Figs. 15,
licerae, would explain theiroften complex and 16). However, inter- and intrasexual functions
species-specific design by physical coercive are not mutually exclusive, and fighting with
mating during which the male has to over- chelicerae must be considered a possibility in
come female resistance and for this purpose single cases.
uses his cheliceral modifications. One predic- Brignoli’s (1973) speculation that pholcid
tion is that one sex (usually the male) changes chelicerae may function to hold the sperm
to increase the match and the other sex during sperm uptake is probably based on the
evolves to either decrease it or it does not observations of Gerhardt (1921-1933, refer-
evolve at ail in that context (Alexander et al. ences in Huber 1998d) that pholcid males
1997, p. 5). The data available for pholcids do make no sperm webs but transfer the drop of
not support this scenario. To the contrary, fe- sperm to the chelicerae and take it up from
male epigyneal structures usually appear ei- there. This hypothesis obviously fails to ex-
ther neutral (flat plates) or even cooperative plain why males should evolve such a variety
(hoods, grooves, pits, scapes) in that they help of modifications to perform the same simple
the male to lodge his chelicerae and thus to task of holding a drop of sperm.
position his body correctly. It should be em- Thus, by elimination, the hypothesis that
phasized that conflict per se is of course not seems to fit the available data best is cryptic
a distinguishing characteristic between the female choice (as also for many other non-
“conflict ofinterest” andthe “femalechoice” genitalic male contact structures - Eberhard
hypotheses. Conflict is a necessary result of 1985). Much like genitalia, chelicerae may
female choosiness, and some morphological function as copulatory courtship devices,
details reflect this conflict particularly clearly: whose elaborate morphology is used to stim-
in a Peruvian pholcid (LD. #2) the male pre- ulate or fit the female in a way that increases
sumably (judging by male and female mor- the male’s chances of fathering her offspring.
phology) lodges his cheliceral apophyses into In this hypothesis two main factors account
a hood in the female epigynum. However, the for the diversity and relatively rapid evolution
138 THE JOURNAL OF ARACHNOLOGY
—
Figures 8-19. Characters discussed in the present paper. 8-9. Epigynum of a Peruvian pholcid (I.D.
#2) in ventral and lateral (anterior side on left) view, showing the median hood and the lateral apophyses;
10-11. Male chelicerae ofthe same species, lateral and frontal view; 12-13. Epigynum, ventral view, and
male chelicerae, frontal view, of 'Blechroscelis' cyaneotaeniata (Keys.); 14. Portrait of an Ecuadorian
species (I.D. #3), with modified fangs; 15-16. Epigynum of the same species, in ventral and lateral
(anterior side on left) view, showing the blind-ended tubes into which the male apophyses are presumably
inserted during copulation; 17-18. Clypeal modifications in two Metagonia species from Peru (17; I.D.
#4) and Brazil (18; I.D. #5); 19. Right pedipalp of a Bolivian species (I.D. #6), in which the patella is
reduced. Drawn to different scales.
HUBER—SEXUAL SELECTION IN PHOLCID SPIDERS 139
of male chelicerae: the unpredictability of fe- gression of FA on size is often interpreted as
male criteria and the neverending competition evidence for handicap models of sexual selec-
among males for access to female eggs. How tion, in which only genetically “good” males
females evaluate the minimal differences can produce display structures that are both
among conspecific males’ chelicerae, i.e,, the large and symmetric (Mpller& Pomiankowski
sensory and neuroanatomical basis for doing 1993; Watson & Thornhill 1994).
so, remains an open question. From a mechanical point ofview, the phol-
Sexual modifications of the male clypeus cid male pedipalp works like a clamp, with
are less common in pholcids, but have appar- the most distal segment (cymbium with pro-
ently evolved several times convergently (e.g., cursus) acting againstthe femur. The economy
in Metagonia: Figs. 17, 18, Holocneminus - of such a clamp is decreased by the two seg-
Huber 1997b, Deeleman-Reinhold 1994). ments in-between (patella, tibia) and could be
Like the chelicerae, the clypeal modifications improved by elimination of one or both seg-
are highly species-specific and in one species ments. In fact, in many pholcids (e.g., in P.
{Metagonia rica Gertsch 1986) it has been globosus), the patella is functionally reduced
shown that they also contact the female gen- in that part of the muscles of the femur insert
&
ital area during copulation (Huber 1997b). in the tibia (Huber Eberhard 1997) and not
A special case of non-genitalic contact as usually in the patella (Ruhl & Rathmayer
structure is the frontal lobe in maleModisimus 1978). And in at least one species (sp. n. from
culicinus (Simon 1893) (Figs. 5, 6). Clypeal Bolivia; I.D. #6) the reduction is complete,
glands open at the lobe, and during copulation with the femur directly articulating with the
the female mouth is in contact with the lobe, tibia and no external trace of the patella left
suggesting gustatorial courtship (Huber (Fig. 19). Yet anothercharacteristic apparently
1997a). However, the nature and function of functioning to increase the force applied to
the gland products are unknown (trigger fe- one critical point is realized in P. globosus
male responses that are favorable to male? - (and probably in all Physocyclus species and
signal the female that copulation has oc- in Artema atlanta Walckenaer 1837): the pro-
curred? - nourish the female?) meaning that a cursi are locked to each other, but the tip of
decision between natural and sexual selection only one is inserted into the female, movedby
is not yet possible (see Eberhard 1996 for ar- the muscular power of both pedipalps (Huber
&
guments linking sexual selection and male Eberhard 1997).
seminal products). Thus, there seems to be an ultimate advan-
tage for males with strong palps, but the prox-
FORCEFUL GENITALIA
imate function of this vigor is poorly under-
Ithas been noted that “details ofcopulatory stood. A possible solution may be in a
courtship often seem to have little relationship structure of the female genitalia that is appar-
to male size or vigor” (Eberhard 1997: 35). If ently unique to pholcids: the so-called
this is the rule, then many pholcids might be “valve”, an often complex “three dimension-
exceptional: their genitalia are obviously their al zipper” between copulatory pouch (uterus
strongest organs (provided with the largest extemus) and oviduct (uterus internus). An
muscles), and in Physocyclus globosus (Tacz. apparent correlation has been documented be-
1873) this force is apparently used to rhyth- tween the strength and complexity of the
mically squeeze parts of the female genitalia “valve” and the strength ofthe male pedipalp
during copulation (Huber & Eberhard 1997). (Huber 1998c). The correlation may be phy-
Moreover, a morphometric study of genitalic logenetically biased, however, so it is difficult
and non-genitalic structures in the same spe- to interpret.
cies also apparently supported the notion that It is not surprising that the recently inten-
there is sexual selection on male vigor: fluc- sified research on pholcids has raised more
tuating asymmetry (FA: deviations from per- questions than it has answered. Thus, I would
fect bilateral symmetry that are thought to re- like to close this short review with yet another
flect the degree of developmental stability) in riddle. The males (but not females) of most
large (strong) genitalia tended to be lower species of several mainly Central American
than in small genitalia (Huber 1996b). In the genera have the femora of their walking legs
recent literature on FA such a negative re- covered with short, almost perpendicularhairs
140 THE JOURNAL OF ARACHNOLOGY
(Huber 1998a), resembling taste hairs (Foelix Elgar, M.A. 1998. Sperm competition and sexual
& Chu-Wang 1973) (Fig. 7). Nothing is selectionin spiders andotherarachnids. Pp. 307-
known of these hairs, apart from the approx- 339. In Sperm Competition and Sexual Selection
imate systematic and geographical distribution (TR. Birkhead & A.R Mpller, eds.). Academic
Press.
of the character, the improbability of taste Foelix, R.E & Chu-Wang I-Wu. 1973. The mor-
hairs being concentrated on femora, and the
phology of spider sensilla. II. Chemoreceptors.
apparent lack of terminal pores necessary for &
Tissue Cell, 5(3):461-478.
chemosensory function. Huber, B.A. 1994. Genitalmorphology, copulatory
ACKNOWLEDGMENTS mechanism and reproductive behaviour in Psil-
ochorus simoni (Borland, 1911) (Pholcidae; Ar-
I thank James Berry, William Eberhard, aneae). Netherlands J. ZooL, 44(l-2):85-99.
Gustavo Hormiga and Brent Opell for valu- Huber, B.A. 1995. Copulatory mechanism in Hol-
able comments on a previous draft. This study ocnemuspluchei and Pholcus opilionoides, with
was supported by a Theodore Roosevelt Fel- notes on male cheliceral apophyses and stridu-
lowship from the American Museum of Nat- latory organs inPholcidae (Araneae). ActaZool.,
ural History, New York. Stockholm, 76:291-300.
Huber, B.A. 1996a. On the distinction between
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