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Evidence of oligogenic sex determination in the apple snail Pomacea canaliculata

DOI:10.1007/s10709-018-0017-z
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Yoichi Yusa at Nara Women's University
Yoichi Yusa
Natsumi Kumagai
Natsumi Kumagai
Natsumi Kumagai
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Abstract and Figures

A small number of genes may interact to determine sex, but few such examples have been demonstrated in animals, especially through comprehensive mating experiments. The highly invasive apple snail Pomacea canaliculata is gonochoristic and shows a large variation in brood sex ratio, and the involvement of multiple genes has been suggested for this phenomenon. We conducted mating experiments to determine whether their sex determination involves a few or many genes (i.e., oligogenic or polygenic sex determination, respectively). Full-sib females or males that were born from the same parents were mated to an adult of the opposite sex, and the brood sex ratios of the parents and their offspring were investigated. Analysis of a total of 4288 offspring showed that the sex ratios of offspring from the full-sib females were variable but clustered into only a few values. Similar patterns were observed for the full-sib males, although the effect was less clear because fewer offspring were used (n = 747). Notably, the offspring sex ratios of all full-sib females in some families were nearly 0.5 (proportion of males) with little variation. These results indicate that the number of genotypes of the full-sibs, and hence genes involved in sex determination, is small in this snail. Such oligogenic systems may be a major sex-determining system among animals, especially those with variable sex ratios.
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Vol.:(0123456789)
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Genetica (2018) 146:265–275
https://doi.org/10.1007/s10709-018-0017-z
ORIGINAL PAPER
Evidence ofoligogenic sex determination intheapple snail Pomacea
canaliculata
YoichiYusa1· NatsumiKumagai1
Received: 2 November 2017 / Accepted: 20 February 2018 / Published online: 26 February 2018
© Springer International Publishing AG, part of Springer Nature 2018
Abstract
A small number of genes may interact to determine sex, but few such examples have been demonstrated in animals, especially
through comprehensive mating experiments. The highly invasive apple snail Pomacea canaliculata is gonochoristic and
shows a large variation in brood sex ratio, and the involvement of multiple genes has been suggested for this phenomenon. We
conducted mating experiments to determine whether their sex determination involves a few or many genes (i.e., oligogenic
or polygenic sex determination, respectively). Full-sib females or males that were born from the same parents were mated to
an adult of the opposite sex, and the brood sex ratios of the parents and their offspring were investigated. Analysis of a total
of 4288 offspring showed that the sex ratios of offspring from the full-sib females were variable but clustered into only a
few values. Similar patterns were observed for the full-sib males, although the effect was less clear because fewer offspring
were used (n = 747). Notably, the offspring sex ratios of all full-sib females in some families were nearly 0.5 (proportion of
males) with little variation. These results indicate that the number of genotypes of the full-sibs, and hence genes involved in
sex determination, is small in this snail. Such oligogenic systems may be a major sex-determining system among animals,
especially those with variable sex ratios.
Keywords Inheritance· Mollusca· Oligogenes· Polygenic sex determination· Sex ratio
Introduction
Sex determination is a basic biological phenomenon in
organisms, as well as an important factor affecting indi-
vidual fitness through sex ratios (Bull 1983; Bachtrog etal.
2014; Beukeboom and Perrin 2014). The population sex
ratio (defined as the proportion of males in a gonochoris-
tic population) is normally stabilized to 0.5 by frequency-
dependent selection for the minor sex (Fisher 1930), and
simple sex-determining systems such as male or female het-
erogamety (XY or ZW sex determination, respectively) often
realize this ratio. Under XY sex determination, for instance,
the genotypes of the offspring are either XY (males) or XX
(females), and the offspring sex ratio is expected to be 0.5 if
an equal number of X- and Y-bearing sperm is produced by
segregation and used for fertilization. However, under more
complex sex determination, the sex ratio may differ from
0.5. For instance, in the platyfish, sex is determined by three
genetic factors, in this case the sex factors X, Y, and W, and
the sex ratio of offspring differs according to the combina-
tion of the parents’ genotypes (Bull 1983; Schultheis etal.
2009). When an XY (male) and a WX (female) mate, the off-
spring are either XY (males) or XX, WX, or WY (females),
and the resulting sex ratio is 0.25 if other parameters such as
mortality are equal. However, mating between a YY (male)
and an XX (female) produces all XY (male) offspring, and
the sex ratio is 1. In this paper, the involvement of such a
small number of factors or genes (usually 3–9) to determine
the sex is termed “oligogenic sex determination”.
Variable sex ratios within a population have been reported
in various animal taxa with genetic sex determination, such
as copepods (Voordouw and Anholt 2002; Foley etal. 2013;
Alexander etal. 2014), mussels (Saavedra etal. 1997; Yusa
etal. 2013; Zouros 2013), polychaetes (Premoli etal. 1996),
and cichlids (Ser etal. 2010). In most cases such variation
in sex ratio is considered to involve many sex-determining
genes. Here, many genes, each with a minor effect, collec-
tively determine an individual’s sex (“polygenic sex deter-
mination”; Bull 1983).
* Yoichi Yusa
yusa@cc.nara-wu.ac.jp
1 Faculty ofScience, Nara Women’s University,
Kitauoya-nishi, Nara630-8506, Japan
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... However, this two-locus model does not fully account for the ratios observed, and a three-locus model proposes that FF produces true females, MM true males, and FM protandric females (Hedgecock and Hedrick 2010). Similar lineage experiments in the dioecious pulmonate, Pomacea canaliculata, have suggested that a small number of genes are required to produce the sex ratios observed in full-and half-sibling crosses (Yusa 2007;Yusa and Kumagai 2018). ...
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