Homosexual behaviour in a cavernicolous fish, Poecilia mexicana (Poeciliidae, Teleostei)

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Zeitschrift für Fischkunde             Band 7            Heft 2          15.09.2005      S. 95-99

                          Homosexual behaviour in a cavernicolous fish,
                            Poecilia mexicana (Poeciliidae, Teleostei)
 Homosexuelles Verhalten bei einem höhlenbewohnenden Fisch, Poecilia mexicana
                             (Poeciliidae, Teleostei)

                           Michael Tobler1*, Karsten Wiedemann2 & Martin Plath2
       1
       Zoologisches Institut der Universität Zürich,Winterthurerstr. 190, CH-8057 Zürich, Schweiz,
                                      michael.tobler@zool.unizh.ch
     2
       Biozentrum Grindel der Universität Hamburg, Martin-Luther-King Platz 3, D-20146 Hamburg,
                                               Deutschland

Summary: We examined male sexual behaviour (nipping) in a cave-dwelling population of a live-bearing
tooth carp, Poecilia mexicana. Two males of different size could interact with a female. The large males
preferentially nipped at the female. In contrast, small males nipped comparably often at the female and at
the male. We discuss a possible function of homosexual interactions in the context of mate choice copying.

Key words: cave fish, live-bearing tooth carp, mating tactic, size polymorphism, mate copying

Zusammenfassung: Wir haben das Sexualverhalten (Nippen) von Männchen eines höhlenbewohnenden
Zahnkärpflings (Poecilia mexicana) untersucht. Zwei unterschiedlich große Männchen konnten jeweils mit
einem Weibchen interagieren. Die großen Männchen nippten bevorzugt am Weibchen. Im Gegensatz dazu
nippten kleine Männchen vergleichbar oft am Weibchen und am Männchen. Wir diskutieren eine mögliche
Funktion homosexueller Interaktionen im Zusammenhang mit der Nachahmung der Partnetwahl.

Schlüsselwörter: Höhlenfisch, Lebendgebärende Zahnkarpfen, Paarungstaktik, Größenpolymorphismus,
Nachahmung der Partnerwahl

1. Introduction                                       with one female (PLATH et al. 2004c). This stu-
                                                      dy has corroborated the finding that large ma-
                                                      les are more sexually active in the cavernico-
A remarkable population of poeciliid fish was         lous form of P. mexicana (PLATH et al. 2003a).
described by GORDON & ROSEN (1962): The At-           This finding was surprising, because in many
lantic molly Poecilia mexicana inhabits a variety     other poeciliids, including the surface form of
of Mexican freshwater habitats, but also a sul-       P. mexicana, small males show more sexual be-
phurous limestone cave in Tabasco, South Me-          haviour, probably as a compensation for their
xico, the Cueva del Azufre. The cave form dif-        disadvantage in female choice (PLATH et al.
fers from surface-dwelling P. mexicana not only       2004a, 2004b) and male-male competition for
in morphological characters like reduced eye-         mates (see PARZEFALL 1974, 1979).
size (PETERS et al. 1973) but also in several be-        Furthermore, in this study (PLATH et al. 2004c)
havioural traits (PARZEFALL 1974, 1979, 1993;         sexual male-male interactions have been observed,
PLATH et al. 2003a).                                  but our former experimental protocol was not
   A previous study has examined the mating           designed to quantify these. Also in several other
behaviour of two cave molly males interacting         studies, sexual interactions between two cave molly

*Address for correspondence: Department of Zoology, University of Oklahoma, 730 Van Vleet Oval,
Norman, OK 73019, USA.
Z. Fischk. Bd. 7 Heft 2

                                                                                                       95
males have been reported (PARZEFALL 1969, 1973),      with his snout. Nipping is the most frequent se-
but to date this behaviour has been given rela-       xual behaviour of P. mexicana males (PARZEFALL
tively little attention. Therefore, the aim of this   1973) and is often followed by copulations.
study was to quantify both hetero- and homose-
xual behaviour in the cave molly. To determine a      3. Results
possible effect of male body size, two different
sized males, a large male and a small one, could      In light, the nipping frequencies differed signifi-
simultaneously interact with a female.                cantly between large and small males and
                                                      between hetero- and homosexual encounters,
2. Material and Methods                               respectively (Friedman test: P0.05, N=6 in both cases).
   The test tank (16 x 23 x 17 cm) was illumina-
ted by two 500 W infrared bulbs during the ob-        4. Discussion
servations in darkness and by an additional 25
W incandescent bulb for the light treatment. To       Our observations showed that small Poecilia me-
initiate a trial, a large male, a small male and a    xicana males nipped comparably often at fema-
female were gently introduced into the test tank      les and at males, whereas large males preferred
and were given five minutes for habituation.          the female. Males can discriminate between
Then, the males’ behaviour was recorded using         males and females when physical contact is
an infrared-sensitive video-camera for 15 min.        possible (ZEISKE 1968, 1971). Hence, homose-
After the first observation, light conditions were    xual behaviour in small cave molly males most
changed and the behaviour was recorded for            likely has a function.
another 15 min in the opposite light treatment.          In another experiment, cave molly males were
We started with the light or with the dark treat-     given an opportunity to associate with a female
ment alternatively. After these observations, the     or an equal sized male. The stimuli were presen-
fish remained in the test tank for 14 hours and       ted either visually, non-visually, or in a combined
the two observations were repeated. We success-       treatment. Discrimination was observed only in
fully tested n = 6 pairs of males.                    the latter treatment, where small males preferred
   Tapes were later analysed. We noted the num-       to associate with the larger male (PLATH et al.
ber of nippings. Nipping was determined as a          2003b). It has been suggested that small males
male touching the genital region of another fish      act as satellites (PLATH et al. 2003b). Given that

96
Fig. 1: Sexual behaviour of cave
molly males. Nipping frequen-
cies of large males (left) and
small males (right) at either a fe-
male or another male. Tests were
carried out in light and in dark-
ness. A second observation was
conducted after 14 h.
Abb 1: Sexualverhalten bei Höh-
lenmollies. Nippfrequenzen gro-
ßer (links) und kleiner Männchen
(rechts) am Weibchen oder am
anderen Männchen. Die Versu-
che wurden in Licht und in Dun-
kelheit durchgeführt. Eine zwei-
te Beobachtung wurde nach 14
h. durchgeführt.

large males are preferred by females (PLATH et al.   (e.g. FIELD & WAITE 2004); but homosexual be-
2004a, 2004b), small males might associate with      haviour may also be adaptive. In P. mexicana, plei-
larger males to increase their mating success.       otropic or sexually antagonistic effects that in-
   This study, however, demonstrates that small      crease fecundity in non-homosexual carriers –
P. mexicana males not only associate with large      and thereby balance the reduction in homose-
males, but even direct sexual behaviour towards      xual fecundity – might explain homosexual be-
the larger male. The persistence of homose-          haviour. Alternatively, sexual behaviour may be
xual behaviour is one of the major and unre-         a signal, and males that exhibit sexual behaviour
solved Darwinian paradoxes (e.g. BELL & WEIN-        may be preferred by females due to mate copy-
BERG 1978). Nonetheless, homosexual beha-            ing (see e.g. SCHLUPP et al. 1994, WITTE & RYAN
viour in the male as well as in the female sex is    1998) – even if they direct sexual behaviour to
known from a wide variety of taxa (BAGEMIHL          another male. This may be a mechanism by which
1999). Several hypotheses attempt to explain         small males increase their attractiveness for fe-
the persistence of homosexual behaviour, ho-         males. Neither the role of the social environ-
wever, empirical data testing the competing          ment, nor antagonistic effects or a function in
ideas are scarce (CAMPERIO -CIANI 2004). It          the context of mate copying have so far been
should be noted that it is not assumed that ho-      studied in cave mollies.
mosexuals never reproduce but that they do              We could observe homosexual behaviour also
reduce, on average, their direct fitness.            in other poeciliid species, however, quantitative
    In many species, male homosexual behaviour       studies remain to be carried out. Male-male nip-
can be induced by altering the social environ-       ping and homosexual copulations could also be
ment such as sexual deprivation from females         observed in surface-dwelling P. mexicana popu-
Z. Fischk. Bd. 7 Heft 2

                                                                                                     97
lations and in the related P. latipinna. Male P. chi-       under varying sperm competition risk in guppies.
ca maintained in single-sex groups copulated with           Anim. Behav. 58, 1001-1006.
each other at high frequency, but this may re-           FIELD, K. L., & T. A. WAITE. 2004. Absence of fema-
flect increased sex-drive after sexual deprivati-           le conspecifics induces homosexual behaviour in
                                                            male guppies. Anim. Behav. 68, 1381-1389.
on. Furthermore, these males were also obser-
                                                         GORDON, M. S., & D. E. ROSEN. 1962. A cavernico-
ved to copulate with heterospecific Heterandria             lous form of the Poeciliid fish Poecilia sphenops from
bimaculata males. In addition, male homosexua-              Tabasco, Mexico. Copeia 1962, 360-368
lity was described for the poeciliids Poecilia reticu-   PARZEFALL, J., 1969. Zur vergleichenden Ethologie
lata (EVANS & MAGURRAN 1999, FIELD & WAITE                  verschiedener Mollienesia-Arten einschließlich ei-
2004), Xiphophorus hellerii and X. maculatus                ner Höhlenform von Mollienesia sphenops. Beha-
(SCHLOSBERG et al. 1949) and other (non-poecili-            viour 33, 1-37.
id) fish species (BAGEMIHL 1999).                        PARZEFALL, J. 1973. Attraction and sexual cycle of
   PARZEFALL (1974, 1979) reported of a striking            poeciliids, pp. 177-183. In: Genetics and mutage-
                                                            nesis of fish (J.H. SCHRÖDER, J.H., ed.). Springer
reduction of aggressive behaviour in the cave
                                                            Berlin, Heidelberg, New York,
molly as compared to surface-dwelling P. mexi-           PARZEFALL, J. 1974. Rückbildung aggressiver Verhal-
cana. In this study, the large male did not prevent         tensweisen bei einer Höhlenform von Poecilia sphe-
the smaller one from nipping at the female even             nops (Pisces, Poeciliidae). Z. Tierpsychol. 35, 66-
after 14 hours, indicating that dominance hier-             84.
archies are absent in this population of P. mexi-        PARZEFALL, J. 1979. Zur Genetik und biologischen
cana. The most striking evidence for reduced ag-            Bedeutung des Aggressionsverhaltens von Poeci-
gression in our study, however, is that the large           lia sphenops (Pisces, Poeciliidae). Z. Tierpsychol.
males even did not prevent smaller males from               50, 399-422.
                                                         PARZEFALL, J. 1993. Schooling behaviour in populati-
sexually interacting with them.
                                                            on-hybrids of Astyanax fasciatus and Poecilia mexica-
                                                            na (Pisces, Characidae and Poeciliidae), pp. 297-303.
5. Acknowledgements                                         In: Trends in Ichthyology: An International Pers-
                                                            pective (SCHRÖDER, H., J. BAUER, & M. SCHARTL, eds).
We thank J. PARZEFALL for helpful discussions.              Blackwell Scientific, Oxford, 297-303.
Financial support came from the University of            PETERS, N., G. PETERS, J. PARZEFALL, & H. WILKENS.
Hamburg to M.P. We are grateful to the Mexi-                1973. Über degenerative und konstruktive Merk-
can Government for issuing the permit to col-               male bei einer phylogenetisch jungen Höhlenform
lect fish (# 242.-2190 276/36). T.H. DIRKS, I.D.            von Poecilia sphenops (Pisces, Poeciliidae). Int. Re-
                                                            vue ges. Hydrobiol. 417-436.
SCHMIDT, A. TAEBEL-HELLWIG and the aquari-
                                                         PLATH, M., K. WIEDEMANN, J. PARZEFALL, & I. SCHLUPP.
um team in Hamburg provided technical sup-                  2003a. Sex recognition in surface and cave dwel-
port and help with fish care.                               ling male Atlantic mollies Poecilia mexicana (Poeci-
                                                            liidae, Teleostei). Behaviour 140, 765-782.
6. Literature                                            PLATH, M., J. PARZEFALL, & I. SCHLUPP. 2003b. The
                                                            role of sexual harassment in cave and surface
BAGEMIHL, B. 1999. Biological exuberance – Animal           dwelling populations of the Atlantic molly, Poeci-
  homosexuality and natural diversity. Profile Books,       lia mexicana (Poeciliidae, Teleostei). Behav. Ecol.
  London.                                                   Sociobiol. 54, 303-309.
BELL, A. P., & WEINBERG, M. 1978. Homosexualities:       PLATH, M., J. PARZEFALL, K. E. KÖRNER, & I. SCHLUPP.
  a study of diversity among men and women. Si-             2004a. Sexual selection in darkness: Female ma-
  mon & Schuster, New York.                                 ting preferences in surface- and cave-dwelling
CAMPERIO-CIANI, A., F. CORNA, & C. CAPILUPPI. 2004.         Atlantic mollies, Poecilia mexicana (Poeciliidae, Te-
  Evidence for maternally inherited factors favou-          leostei). Behav. Ecol. Sociobiol. 55, 596-601.
  ring male homosexuality and promoting female           PLATH, M., M. TOBLER, & I. SCHLUPP. 2004b. Cave fish
  fecundity. Proc. R. Soc. LOND. B 271: 2217-21             looking for mates: a visual mating preference in
EVANS, J. P., & A. E. MAGURRAN. 1999. Male mating           surface- and cave-dwelling Atlantic mollies (Poecilia
  behaviour and sperm production characteristics            mexicana, Poeciliidae). Z. Fischk. 7, 61-69.

98
PLATH, M., M. ARNDT, J. PARZEFALL, & I. SCHLUPP.              ZEISKE, E. 1968. Prädispositionen bei Mollienesia sphe-
   2004c. Size-dependent male mating behaviour in                nops (Pisces, Poeciliidae) für einen Übergang zum
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SCHLOSBERG, H., M. C. DUNCAN ,& B. DAITCH. 1949.              ZEISKE, E. 1971. Ethologische Mechanismen als Vo-
   Mating behavior of two life-bearing fish Xipho-               raussetzung für einen Übergang zum Höhlenle-
   phorus helleri [sic] and Platypoecilus maculatus. Physi-      ben. Untersuchungen an Kaspar-Hauser-Männ-
   ol. Zool. 22, 148-161.                                        chen von Poecilia sphenops (Pisces, Poeciliidae).
SCHLUPP, I., C. A. MARLER , & M. J. RYAN. 1994. Bene-            Forma et functio 4, 387-393.
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   fluences mate-choice copying in the sailfin molly          Received : 23.11. 2004
   Poecilia latipinna. Behav. Ecol. 9, 534-539.               Accepted : 19.01.2005

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