1624
MARIE-FRANCE OSTROWSKI ET AL.
Bell, G. 1982. The masterpiece of nature: the evolution and genetics
of sexuality. Univ. of California Press, Berkeley.
Brown, D. S. 1994. Freshwater snails of Africa and their medical
importance. Taylor and Francis Ltd., London.
Bull, J. J., and E. L. Charnov. 1989. Enigmatic reptilian sex ratios.
Evolution 43:1561–1566.
Couvet, D., A. Atlan, E. Belhassen, C. Gliddon, P.-H. Gouyon, and
F. Kjellberg. 1990. Co-evolution between two symbionts: the
case of cytoplasmic male-sterility in higher plants. Oxf. Surv.
Evol. Biol. 7:225–249.
indeed requires a thorough description of genotype-by-en-
vironment interactions, as the latter allow not only for se-
lection on plasticity, but also for the maintenance of vari-
ability in natural populations subject to macroenvironmental
variation.
With regard to aphally, the adaptive nature of plasticity
remains unknown because the selective forces involved have
not been characterized in natural populations. This situation
parallels that of environmental sex determination, for which Crawley, M. J. 1993. GLIM for ecologists. Blackwell Scientific
Publications, Oxford, U.K.
adaptive hypotheses received ambiguous support from em-
pirical data (Bull and Charnov 1989; Rhen and Lang 1998).
Darwin, C. R. 1877. The different forms of flower on plants of the
same species. Murray, London.
In the current models, the evolution of aphally depends on
Deng, H.-W. 1997. Increase in developmental instability upon in-
natural selection on selfing rates, that is, inbreeding depres-
sion, the cost of the male function, and the shape of the
relationship between the selfing rate and AR (Doums et al.
1998b). Because the range of values for these parameters in
B. truncatus is not yet well assessed, the relevant selective
pressures acting on ARs are still uncertain. Sensitivity of the
sexual morph to temperature has to be added to this list of
parameters. Indeed, temperature may correlate with condi-
tions under which selfing is selected. Schrag et al. (1994a)
detected a correlation between AR and parasitic prevalence
in Nigerian populations of B. truncatus and proposed that
euphallic individuals would be favored at low temperatures
if the parasitic pressure increases when temperature decreas-
es. This hypothesis assumes that outcrossed progeny have a
better fitness than selfed progeny in the presence of parasites,
as suggested by the Red Queen hypothesis (Bell 1982). How-
ever, many parameters other than parasitic pressure, such as
population density or metabolic maintenance costs, may cor-
relate with temperature and modify the selective pressure on
aphally. These hypotheses remain ad hoc speculations in the
absence of relevant data. However, because Bulinus popu-
lations are unstable and frequently experience bottlenecks
(Brown 1994; Vera et al. 1994; Viard et al. 1997), short-term
patterns at the scale of one or a few natural populations may
reflect recent random events rather than equilibrium situa-
tions optimized by natural selection.
breeding in Daphnia. Heredity 78:182–189.
Doums, C., and P. Jarne. 1996. The evolution of phally polymor-
phism in Bulinus truncatus (Gastropoda, Planorbidae): the cost
of male function analysed through life-history traits and sex
allocation. Oecologia 106:464–469.
Doums, C., P. Bre´mond, B. Delay, and P. Jarne. 1996a. The ge-
netical and environmental determination of phally polymor-
phism in the freshwater snail Bulinus truncatus. Genetics 142:
217–225.
Doums, C., R. Labbo, and P. Jarne. 1996b. Stability and genetical
basis of variability of phally polymorphism in natural popula-
tions of the self-fertile freshwater snail Bulinus truncatus. Genet.
Res. Camb. 68:22–33.
Doums, C., M.-A. Perdieu, and P. Jarne. 1998a. Resource allocation
and stressful conditions in the aphallic snail Bulinus truncatus.
Ecology 79:720–733.
Doums, C., F. Viard, and P. Jarne. 1998b. The evolution of phally
polymorphism. Biol. J. Linn. Soc. 64:273–296.
Eanes, W. F. 1978. Morphological variance and enzyme hetero-
zygosity in the monarch butterfly. Nature 276:263–264.
Falconer, D., S., and T. F. C. Mackay. 1996. Introduction to quan-
titative genetics. Longman.
Gavrilets, S., and A. Hastings. 1994. A quantitative model for se-
lection on developmental noise. Evolution 48:1478–1486.
Gouyon, P. H., F. Vichot, and J. M. M. Van Damme. 1991. Nuclear-
cytoplasmic male sterility: single-point equilibria versus limit
cycles. Am. Nat. 137:498–514.
Hazel, W. N., R. Smock, and M. D. Johnson. 1990. A polygenic
model for the evolution and maintenance of conditional strate-
gies. Proc. R. Soc. Lond B Biol. Sci. 242:181–187.
Janzen, F. J. 1992. Heritable variation for sex ratio under environ-
mental sex determination in the common snapping turtle (Che-
lydra serpentina). Genetics 131:155–161.
Janzen, F. J., and G. L. Paukstis. 1991. Environmental sex deter-
mination in reptiles: ecology, evolution, and experimental de-
sign. Q. Rev. Biol. 66:149–179.
Jarne, P., L. Finot, C. Bellec, and B. Delay. 1992. Aphally versus
euphally in self-fertile hermaphrodite snails from the species
Bulinus truncatus (Pulmonata: Planorbidae). Am. Nat. 139:
424–432.
Larambergue, M. de 1939. Etude de l’autofe´condation chez les gas-
te´ropodes pulmone´s: recherches sur l’aphallie et la fe´condation
chez Bulinus (Isidora) contortus Michaud. Bull. Biol. Fr. Belg.
73:19–231.
Lerner, I. M. 1954. Genetic homeostasis. Oliver and Boyd, London.
Lynch, M., and B. Walsh. 1998. Genetics and analysis of quanti-
tative traits. Sinauer, Sunderland, MA.
A
CKNOWLEDGMENTS
We thank C. Doums, F. Justy, M.-A. Perdieu, and F. Viard,
whose help was invaluable for maintaining the snail lines;
C. Doums for discussions; and C. Doums and two anonymous
reviewers for comments on the manuscript. This work was
supported by funds from the Centre National de la Recherche
Scientifique (CNRS) to UMR 5554 (Institut des Sciences de
l’Evolution) and UPR 9056 (Centre d’Ecologie Fonctionnelle
et Evolutive). This work is part of the Ph.D. project of M-
FO, which is supported by funds from the Natural Sciences
and Engineering Research Council of Canada (NSERC).
McCullagh, H. P., and J. A. Nelder. 1983. Generalized linear mod-
els. Cambridge Univ. Press, Cambridge.
Mitton, J. B. 1978. Relationship between heterozygosity forenzyme
loci and variation of morphological characters in natural pop-
ulations. Nature 273:661–662.
L
ITERATURE CITED
Baker, R. J., and J. A. Nelder. 1985. The GLIM system. Rel. 3.77,
manual. Numerical Algorithms Group, Oxford, U.K.
Barrett, S. C. H. 1994. The evolutionary biology of tristyly. Oxf. Paoletti, C., and K. E. Holsinger. 1999. Spatial patterns of polygenic
Surv. Evol. Biol. 9:283–326.
Baur, B., X. Chen, and A. Baur. 1993. Genital dimorphism in natural
variation in Impatiens capensis, a species with an environmental
controlled mixted mating system. J. Evol. Biol. 12:689–696.
populations of the land snail Chondrina clienta and the influence Rhen, T., and J. W. Lang. 1998. Among-family variation for en-
of the environment on its expression. J. Zool., Lond. 231:
275–284.
vironmental sex determination in reptiles. Evolution 52:
1514–1520.