the effects of body size on mating features in a field population of the ...

Moll Stud. (1996), 62, 381-386 O The Malacological Society <strong>of</strong> London 1996
THE EFFECTS OF BODY SIZE ON MATING FEATURES IN A
FIELD POPULATION OF THE HERMAPHRODITIC SEA
HARE APLYS1A KURODAI BABA, 1937 (GASTROPODA:
OPISTHOBRANCHIA)
YOICHI YUSA
Sew Marine Biological Laboratory, Faculty <strong>of</strong> Science, Kyoto Umvenity, Shirahama, Wakayama 649-22, Japan
(Received 27 November 1995, accepted 8 February 1996)
ABSTRACT
Mating behaviour <strong>of</strong> <strong>the</strong> hermaphroditic sea hare
Aplysia kurodai Baba was observed in <strong>the</strong> field to
investigate <strong>the</strong> <strong>effects</strong> <strong>of</strong> <strong>body</strong> <strong>size</strong> on various mating
features. Compared with small individuals, large gastropods
mated with more partners both as males and
as females, and also with larger partners (<strong>size</strong>-assortative
mating). Large gastropods also mated more
frequently as females but not as males, and tended to
be selected as female mating partners more <strong>of</strong>ten
than small ones by neighbouring individuals but not
as male partners. All <strong>the</strong>se results suggest some mating
advantage <strong>of</strong> large individuals over small ones as
females, probably because <strong>of</strong> <strong>the</strong> preference by male
partners for large female partners. At <strong>the</strong> same time,
<strong>the</strong> results suggest that <strong>the</strong> mating advantage <strong>of</strong> large
<strong>size</strong> as males may be limited, if any. The preference
for large female partners is also consistent with <strong>the</strong>
fact that <strong>the</strong>ir mating was longer than that <strong>of</strong> small
ones. The greater advantage <strong>of</strong> large <strong>size</strong> in mating
as females, than as males, means that sexual selection
at mate determination acts more strongly on
female <strong>size</strong> than on male <strong>size</strong> and that <strong>the</strong> direction
<strong>of</strong> total sexual selection at mating is probably
reversed in this hermaphrodite
INTRODUCTION
In <strong>the</strong> majority <strong>of</strong> gonochoric (separate sexes)
animals, males are more competitive in obtaining
<strong>the</strong>ir mates than females, and/or females
are more choosy about <strong>the</strong>ir mates than males
(Darwin, 1871). As a result, sexual selection
acts more strongly on males at mate determination
(postmating sexual selection is not
treated in this paper). However, in a small
number <strong>of</strong> gonochoric insects, crustaceans and
vertebrates, females are known to be more
competitive and/or less choosy than males and
sexual selection acts more strongly on females
(reviewed in Gwynne, 1991; Clutton-Brock &
Vincent, 1991). These instances <strong>of</strong> reversed
sexual selection have been used to test current
<strong>the</strong>ones on <strong>the</strong> causes <strong>of</strong> sexual selection
(Williams, 1966; Tnvers, 1972, 1985; Clutton-
Brock & Vincent, 1991; Gwynne, 1991; Vincent,
Ahnesjo, Berglund & Rosenqvist, 1992).
Also in most simultaneous hermaphrodites
(combined sexes), sexual selection is believed
to act more strongly on male function than on
female function (Charnov, 1979). In fact, <strong>the</strong>re
have been virtually no reports demonstrating
stronger sexual selection on female function
than on male function in simultaneous
hermaphrodites, except in a laboratory study
on <strong>the</strong> sea hare Aplysia kurodai Baba, 1937
(Yusa, 1995). The purpose <strong>of</strong> this study was to
investigate whe<strong>the</strong>r <strong>the</strong> direction <strong>of</strong> sexual
selection is also reversed in a field population
<strong>of</strong> <strong>the</strong> sea hare. The <strong>effects</strong> <strong>of</strong> <strong>body</strong> <strong>size</strong> on features
concerning mating success are stressed,
since large <strong>body</strong> <strong>size</strong> is <strong>of</strong>ten advantageous
under sexual selection (Ridley, 1983; Trivers,
1985; Andersson, 1994). This should be particularly
true for gastropods that lack conspicuous
<strong>body</strong> colour or exaggerated sexual
ornaments typically found in vertebrates or
insects. In fact, several studies have reported
<strong>the</strong> <strong>effects</strong> <strong>of</strong> <strong>body</strong> <strong>size</strong> on various mating features
in gastropods (Crozier, 1918; Edwards,
1968; Otsuka, Rouger & Tobach, 1980;
Erlandsson & Johannesson, 1994; Yusa, 1994a,
1995; Staub & Ribi, 1995). The sea hare
Aplysia kurodai has a dark <strong>body</strong> colour with
no conspicuous sexual ornaments. Thus if <strong>the</strong>
direction <strong>of</strong> sexual selection is reversed, <strong>the</strong>
advantage <strong>of</strong> large <strong>body</strong> <strong>size</strong> should be greater
in female function than in male function <strong>of</strong> this
hermaphrodite.
MATERIALS AND METHODS
During mating, an individual <strong>of</strong> Aplysia acting as a
male mounts ano<strong>the</strong>r one acting as a female. When
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382 Y. YUSA
more than two individuals participate in mating, <strong>the</strong>y
<strong>of</strong>ten form a copulatory chain, in which <strong>the</strong> first individual
acts as a female, <strong>the</strong> last as a male, and those
in between both as males and as females. In A. kurodai,
alternation <strong>of</strong> mating roles between two partners
is rarely observed, representing only 5% <strong>of</strong> total
mating instances (Yusa, 1995). In this study, one
mating means a copulatory bond between a male
partner and a female partner. Thus, for example, a
copulatory chain consisting <strong>of</strong> three individuals contains
two matings.
A series <strong>of</strong> field observations were made for 3
days (74 hours) in May 1989, on a rocky shore near
<strong>the</strong> Seto Marine Biological Laboratory in sou<strong>the</strong>rn
central Japan (33° 41' N, 135° 20' E). Two tide pools
(one with surface area <strong>of</strong> 180 m 2 and <strong>the</strong> o<strong>the</strong>r <strong>of</strong> 2
m 2 ), situated close to each o<strong>the</strong>r, were chosen for <strong>the</strong>
study. Sea hares could move between <strong>the</strong> two pools
almost freely during high tides, and <strong>the</strong> movement
between <strong>the</strong> pools was recorded 14 times in 3 days.
All <strong>the</strong> 26 individuals <strong>of</strong> A. kurodat found in <strong>the</strong>
study area were individually tagged with small plastic
labels (Nishiwalci, Ueda & Makioka, 1975) before
observations. During <strong>the</strong> 3-day period, a total <strong>of</strong> 51
observations were made at 1 or 2-hour intervals. An
electric torch was used for night observations. In
each observation <strong>the</strong>ir locations in <strong>the</strong> study area
and mating partners, if mating, were recorded. Since
intromission <strong>of</strong> <strong>the</strong> penis was not visible in most
cases, an individual was assumed to be mating as a
male when it was mounting ano<strong>the</strong>r individual, with
its head attaching firmly between <strong>the</strong> parapodia <strong>of</strong>
<strong>the</strong> mounted partner and without major movement
for at least 15 seconds.
Because some individuals were missing in some
observations, each individual was observed in 93 i
9.7% (mean ± SD) <strong>of</strong> total observations. This proportion
had no significant correlation with <strong>the</strong> <strong>body</strong>
<strong>size</strong> <strong>of</strong> individuals (N = 26, r = 032, P > 0.1). A
mating bout was assumed to have started at <strong>the</strong> middle
<strong>of</strong> <strong>the</strong> observation interval before it was
observed first and to have ended at <strong>the</strong> middle <strong>of</strong> <strong>the</strong>
interval after it was witnessed last. Likewise, two
matings that were witnessed in <strong>the</strong> first observation
<strong>of</strong> <strong>the</strong> study period were assumed to have started
half an hour before <strong>the</strong> observation, but no matings
were found in <strong>the</strong> last observation. In two cases,
however, both <strong>of</strong> <strong>the</strong> mating partners failed to be
observed in one <strong>of</strong> such consecutive observations in
which <strong>the</strong>y were found mating in <strong>the</strong> same roles. In
<strong>the</strong>se cases <strong>the</strong> partners were considered to be mating
continuously even when <strong>the</strong>y were not observed.
The <strong>body</strong> volume <strong>of</strong> individuals was measured by
water displacement before and after <strong>the</strong> observation
period, and <strong>the</strong> mean <strong>of</strong> <strong>the</strong> two values was adopted
as <strong>the</strong>ir <strong>body</strong> <strong>size</strong>. For five individuals that were not
found at <strong>the</strong> second measurement, <strong>the</strong> corresponding
<strong>body</strong> <strong>size</strong> was calculated based on <strong>the</strong> average
growth rate (an 8% increase) <strong>of</strong> <strong>the</strong> individuals measured
twice. At <strong>the</strong> second measurement, <strong>the</strong>ir <strong>body</strong>
weight was measured toge<strong>the</strong>r with <strong>body</strong> volume,
and it showed a highly positive correlation with <strong>body</strong>
volume (N - 21, r =» 0.998, P < 0.001).
RESULTS
Mating frequency and <strong>the</strong> number <strong>of</strong> different
partners
A total <strong>of</strong> 26 individuals <strong>of</strong> A. kurodai (mean
± SD <strong>body</strong> volume = 46 ± 19 ml) performed
89 matings during <strong>the</strong> 3-day observation
period. In addition, four <strong>of</strong> <strong>the</strong>m were
observed to mate with a large (208 ml) individual
<strong>of</strong> A dactylomela Rang eight times in total,
and in each case A kurodai acted as a male.
These interspecific matings are excluded from
fur<strong>the</strong>r analyses.
AJ1 <strong>the</strong> 26 individuals acted as females during
<strong>the</strong> observation period, and all except <strong>the</strong>
smallest and a middle-<strong>size</strong>d one (53 ml) acted
as males (but <strong>the</strong> latter individual acted as a
male twice with A dactylomela). The sea hares
on average mated 1.2 times per day per individual
as each sex, and <strong>the</strong> standard deviation
<strong>of</strong> daily mating frequency among individuals
(0.6O) was identical between <strong>the</strong> sexes. Large
individuals mated more frequently than small
ond as females (Fig. 1; N = 26, r = 0.57, P <
0.01), but as males mating frequency had no
significant correlation with <strong>body</strong> <strong>size</strong> (r = 033,
P > 0.1).
Sea hares were observed to mate with on
average 2.6 different partners as each sex in 3
days, and <strong>the</strong> standard deviation was slightly
greater in <strong>the</strong> male than in <strong>the</strong> female (13 vs.
1.2). The number <strong>of</strong> different partners was
positively correlated with <strong>body</strong> <strong>size</strong> in mating
as males (Fig. 2; r = 0.48; P < 0.05) and even
more strongly in mating as females (r = 0.72, P
< 0.001).
Sizes <strong>of</strong> partners
A kurodai showed a weak tendency <strong>of</strong> <strong>size</strong>assortative
mating (Fig. 3; N = 89, r = 0.21, P
< 0.05). However, combinations <strong>of</strong> a large
male partner and a small female partner, or <strong>of</strong>
a small male partner and a large female partner,
were occasionally observed.
Mating duration
The mating duration in this sea hare was 5.6 ±
4.8 hours (mean ± SD, N = 89), with <strong>the</strong>
longest being 24 hours (Fig. 4). Since <strong>the</strong> mating
durations were not normally distributed,
<strong>the</strong>y were transformed into natural logarithms
before analyzed statistically. When a multiple
regression was conducted using both male and
female <strong>body</strong> <strong>size</strong>s as independent variables,
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10 20 30 40 50 60 70
Body <strong>size</strong> (ml)
MATING BEHAVIOUR OF APLYSIA 383
80
1
3
2
1
n Jo
- Female
-
#
*•
i i i i
s
• • t
I i
10 20 30 40 50 60 70 80
Body <strong>size</strong> (ml)
Figure 1. Mating frequency as males and as females in relation to <strong>body</strong> <strong>size</strong> Since <strong>the</strong> number <strong>of</strong> matings actually
observed is related almost linearly with <strong>the</strong> proportion <strong>of</strong> successful observations on each individual to
<strong>the</strong> total 51 observations, <strong>the</strong> mating frequency is corrected as <strong>the</strong> number <strong>of</strong> matings per day divided by <strong>the</strong>
proportion.
10 20 30 40 50 60 70 80
Body <strong>size</strong> (ml)
10 20 30 40 50 60 70 80
Body <strong>size</strong> (ml)
Figure 2. Relationship <strong>of</strong> <strong>body</strong> <strong>size</strong> to number <strong>of</strong> different partners in matings as males and as females
10 20 30 40 50 60
Male <strong>body</strong> <strong>size</strong> (ml)
70
Figure 3. Relationship between <strong>body</strong> <strong>size</strong>s <strong>of</strong> male
and female partners.
increasing female <strong>size</strong> had a significant positive
effect (P < 0.05) while increasing male <strong>size</strong>
had a nearly significant negative effect (P =
0.05).
Partner determination among neighbouring
individuals
In 73 <strong>of</strong> 77 matings (95%) in which <strong>the</strong> locations
<strong>of</strong> both male and female partners had
been known in <strong>the</strong> observation just before <strong>the</strong>y
began to mate, <strong>the</strong> distance between <strong>the</strong> partners
had been less than 15 m at that tune.
Within this range, whe<strong>the</strong>r a focal individual,
ei<strong>the</strong>r prospective male or female mating partner,
tended to mate with a larger individual
(above <strong>the</strong> median) or with a smaller one
(below it) among its possible mating partners
was analyzed. The possible partners <strong>of</strong> <strong>the</strong>
focal individual were those which were within
15 m <strong>of</strong> it and were not mating as <strong>the</strong> same sex
a
»
i
#
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384 Y.YUSA
2 4 6 8 10 12 14 16 18 20 22 24
Mating duration (h)
Figure 4. Frequency distnbution <strong>of</strong> matings with various durations.
Table 1.'Partner determination by <strong>size</strong> among possible candidates
within 1.5 m. Tendencies <strong>of</strong> selecting large or small mating partners
were tested against <strong>the</strong> null hypo<strong>the</strong>sis <strong>of</strong> no-discrimination (a 1:1
choice). Total data <strong>size</strong> was less than 73 for each sex because <strong>of</strong> <strong>the</strong>
exclusion <strong>of</strong> matings without candidates o<strong>the</strong>r than <strong>the</strong> actual mating
partner.
Partner selected from:
Large Median Small Binomial test
Focal individual is:
Male 33 3 8 P < 0.05
Female 19 4 15 P >0.6
as its actual partner when <strong>the</strong> mating was supposed
to occur.
Male partners tended to mate with a large
female partner more <strong>of</strong>ten than with a small
one (Table 1). In contrast, female partners did
not choose large or small male partners preferentially
among possible candidates.
DISCUSSION
In this study individuals were observed once
per 1 or 2 hours. Thus some <strong>of</strong> <strong>the</strong> matings
shorter than 2 hours must have been overlooked
However, <strong>the</strong>se overlooked matings
may play only a minor role in understanding
<strong>the</strong> mating system <strong>of</strong> A. kurodai for two reasons.
Firstly, <strong>the</strong> proportion <strong>of</strong> matings lasting
for £ 2 hours in this study (35/89 = 39%) did
not differ much from that observed in <strong>the</strong> laboratory
(47%), where all <strong>the</strong> matings £ 3 minutes
were recorded (Yusa, 1995). Secondly, in
this species only 1/5 <strong>of</strong> <strong>the</strong> matings lasting for £
2 hours involve actual sperm transfer into <strong>the</strong>
recipient, whereas all <strong>the</strong> longer matings did so
(Yusa, 1996). Thus mating pattern observed in
this study probably reflects actual sperm transfer
events.
Several lines <strong>of</strong> evidence suggest that large
individuals <strong>of</strong> A. kurodai had some advantage
over small ones in mating as females. Firstly,
large individuals mated more frequently as
females (Fig. 1) and <strong>the</strong>y mated with more
partners (Fig. 2) than small ones. Secondly,
male partners tended to mate with large
female partners more <strong>of</strong>ten than with small
female partners among possible candidates
within 1J m (Table 1). Moreover, <strong>size</strong>-assortative
mating (Fig. 3) may also suggest mating
advantage <strong>of</strong> large female partners (Ridley,
1983; Crespi, 1989; Erlandsson & Johannesson,
1994). Since competition between female partners
has not been observed in this species,
<strong>the</strong>se results suggest that <strong>the</strong> advantage <strong>of</strong>
large female partners was because <strong>of</strong> <strong>the</strong> preference
by male partners for <strong>the</strong>m. Longer matings
by large female partners than small ones
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are also consistent with <strong>the</strong> male partners'
preference for large female partners (Yusa,
1994a). Spatial or temporal distributions <strong>of</strong>
individuals (Edwards, 1968; Ridley, 1983;
Crespi, 1989; Erlandsson & Johannesson, 1994;
Staub & Ribi, 1995) axe not <strong>the</strong> sole causes <strong>of</strong>
non-random mating in A. kurodai, since <strong>the</strong>
tendency <strong>of</strong> non-random mating was evident
even when <strong>the</strong> pattern <strong>of</strong> partner determination
was examined for each mating in <strong>the</strong>
range <strong>of</strong> 1.5 m (Table 1). Any mechanical constraints
for pairing between partners <strong>of</strong>
unequal <strong>size</strong>s (Crozier, 1918; Edwards, 1968)
seem not to exist, as matxngs between partners
<strong>of</strong> unequal <strong>size</strong>s were <strong>of</strong>ten observed (Fig. 3).
The reason why male partners prefer large
female partners may be a higher reproductive
success, as large individuals lay more eggs than
small ones (Yusa, 1994b). The finding by
Otsuka et aL (1980) that <strong>the</strong> female partner
tended to be larger than <strong>the</strong> male partner in
mating pairs <strong>of</strong> A. puntata Cuvier found in <strong>the</strong>
field is also explicable by more frequent matings
and/or longer mating durations by large
female partners.
On <strong>the</strong> o<strong>the</strong>r hand, a large <strong>body</strong> <strong>size</strong> seems
to be <strong>of</strong> minor, if any, advantage to a male
partner. Results supporting this type <strong>of</strong> advantage
are a positive correlation between <strong>body</strong>
<strong>size</strong> and number <strong>of</strong> different partners in mating
as males (Fig. 2) and a weak tendency <strong>of</strong>
<strong>size</strong>-assortative mating (Fig. 3). Note that <strong>the</strong>
former correlation was weaker than <strong>the</strong> corresponding
correlation as females (Fig. 2).
A higher mating frequency <strong>of</strong> large individuals
acting as females but not when acting as
males (Fig. 1), toge<strong>the</strong>r with o<strong>the</strong>r pieces <strong>of</strong>
evidence suggesting mating advantage <strong>of</strong> large
<strong>size</strong> as females and limited advantage as males
(Figs. 2,3; Table 1), mean that sexual selection
at mate determination acts more strongly on
female <strong>size</strong> than on male <strong>size</strong> in A. kurodai.
Since this sea hare has dark <strong>body</strong> colour and
no conspicuous sexual ornaments, sexual selection
operating on <strong>the</strong>se characters probably
has only negligible <strong>effects</strong>. Then, total sexual
selection should also act more strongly on
female function than on male function. This
conclusion is consistent with a laboratory study
on this species reporting stronger sexual selection
on female <strong>size</strong> than on male <strong>size</strong> (Yusa,
1995). Moreover, <strong>the</strong> laboratory study also
showed that <strong>the</strong> variance <strong>of</strong> mating frequency,
i.e. <strong>the</strong> 'opportunity for sexual selection'
(Andersson, 1994), was greater in mating as
females than in mating as males. In <strong>the</strong> present
field study, however, <strong>the</strong> standard deviation,
MATING BEHAVIOUR OF APLYSIA 385
and hence <strong>the</strong> variance <strong>of</strong> mating frequencies
(036), were identical between <strong>the</strong> sexes.
When a local sex ratio is not female-biased,
<strong>the</strong> occurrence <strong>of</strong> reversed sexual selection
requires some expenditure by male partners
such as paternal care or nuptial gifts (Williams,
1966; Trivers, 1972, 1985; Clutton-Brock &
Vincent, 1991; Gwynne, 1991; Vincent et a/.,
1992). Although no parental care, ei<strong>the</strong>r paternal
or maternal, has been known in Aplysia, a
portion <strong>of</strong> <strong>the</strong> sperm received during mating is
in fact digested (Beeman, 1970a, 1970b, 1977;
Brandriff & Beeman, 1973) and hence can be
regarded as a nuptial gift (Charnov, 1979).
Thus, it is concluded that reversal in sexual
selection at mating occurs in a field population
<strong>of</strong> A. kurodai, judged by (1) stronger sexual
selection on female <strong>size</strong> than on male <strong>size</strong>, (2)
similar variance <strong>of</strong> mating frequency as
females and as males, which indicates that <strong>the</strong>
opportunity for sexual selection is at least not
male-biased as in most animals, and (3) <strong>the</strong>
presence <strong>of</strong> sperm digestion, which can be <strong>the</strong>
potential cause <strong>of</strong> this reversal. Reversed sexual
selection has been reported in several
gonochoric animals (reviewed in Gwynne,
1991; Clutton-Brock & Vincent, 1991). In addition,
Erlandsson & Johannesson (1994) have
reported that sexual selection on <strong>body</strong> <strong>size</strong> acts
more strongly on females than on males in a
gonochoric gastropod, Littorina littorea (L.).
On <strong>the</strong> o<strong>the</strong>r hand, <strong>the</strong>re has been no o<strong>the</strong>r
hermaphrodites in which reversal in sexual
selection is claimed to occur. However, in <strong>the</strong>
opisthobranch Navanax inermis (Cooper),
Leonard & Lukowiak (1984, 1985, 1991) have
shown that individuals are less inclined to act
as males than as females given <strong>the</strong> choice to
act as ei<strong>the</strong>r sex. This means that each individual
is more choosy about its mating partners as
a male than as a female and hence can be
regarded as evidence <strong>of</strong> reversed sexual selection.
Although studies on <strong>the</strong> sexual selection
in hermaphroditic gastropods have been few,
in a pulmonate Achatina fulica (Fdrussac) sexual
selection appears to act more strongly on
male function than on female function
(Tomiyama, 1994), unlike in Aplysia or
Navanax. In ano<strong>the</strong>r pulmonate Arianta arbustorum
(L.), sexual selection does not appear to
act on ei<strong>the</strong>r sex, probably due to time-constrained
activity and high costs <strong>of</strong> finding
mates (Baur, 1992). This variability in <strong>the</strong>
direction and intensity <strong>of</strong> sexual selection
makes hermaphroditic gastropods one <strong>of</strong> <strong>the</strong>
model systems to investigate <strong>the</strong> causes <strong>of</strong> sexual
selection (Leonard, 1991).
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386 Y.YUSA
ACKNOWLEDGEMENTS
I wish to thank Drs. Naoya Abe, Eiji Harada,
Masahiko Higashi, Michio Hori, Michio Imafuku,
Tamiji Inoue, Kerstin Johannesson,
Janet L. Leonard, Shigeyuki Yamato and an
anonymous reviewer for <strong>the</strong>ir critical reading
<strong>of</strong> various versions <strong>of</strong> this manuscript. I am
deeply indebted to Pr<strong>of</strong>. Eiji Harada for his
invaluable advice during <strong>the</strong> course <strong>of</strong> this
study.
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