Download Heritable Variation for Female Mating Frequency in Field Crickets

Behavioral Ecology
and Sociobiology
Behav Ecol Sociobiol (1990) 26:73-76
? Springer-Verlag
1990
Heritable variation for female mating frequency
in field crickets, Gryllus integer
Bernt D. Solymar and William H. Cade
Departmentof Biological Sciences, Brock University, St. Catharines,Ontario, Canada L2S 3A1
Received April 20, 1989 / Accepted August 7, 1989
Summary. Female mating frequency was studied
in the laboratory in field crickets, Gryllus integer.
Females mated 9.8 times on average (N= 46, SD =
6.6, range= 1-30) in 10-day observations of 5 h
each. Offspring from each female were raised and
the mating frequencydeterminedfor 10 female offspring from each family. Female offspring mated
from 0 to 26 times. The average number of matings
across all families was 7.3 (SD = 3.4, range
1.9-16.2). Regression of daughter mating frequency on mother mating frequency resulted in
a statistically significant slope of 0.345 and a narrow sense heritability estimate of 0.69 (SE= 0.29).
Additive genetic variation is available for selection
on female mating frequency in G. integer. Results
are discussed in terms of selection on female mating frequency.
Introduction
Female insects of many species mate repeatedly
and store sperm from previous matings. Repeated
mating in Drosophilamelanogasterensures an adequate supply of spermatozoa (Pyle and Gromko
1978). In some species, however, the benefits of
multiple mating to females are unclear since females may mate more times than is necessary to
provide sufficient spermatozoa for fertilization of
all or most of a female's eggs (Parker 1970; Sivinski 1980; Walker 1980). Mating may also be
costly to females since sexual behavior results in
increased exposure to predators and parasites, utilizes time and energy, and may result in physical
damage (Borgia 1981; Sakaluk and Belwood 1984;
Wing 1988). Depending on the species, some advantages of multiple mating in female insects include acquisition of male-controlled resourcessuch
Offprint requests to.* W.H. Cade
as prey items or flowers located in male territories,
and acquisition of male-produced resources such
as spermatophores and spermatophylaxes that
provide nutrition as well as spermatozoa (Gwynne
1984; Sakaluk 1984, 1987; Sakaluk and Cade 1980,
1983; Simmons 1988; Thornhill 1976; Thornhill
and Alcock 1983). An alternative view is that female insects express genes for increasedmating frequency that have been selected for in conspecific
males, but that are neutral or under less strong
selection in females (Halliday and Arnold 1987;
Arnold and Halliday 1988; but see Sherman and
Westneat 1988). In both hypotheses, phenotypic
variation is assumed or stated to correlate with
underlying additive genetic variation. That is, proposals that multiple mating is beneficial to females
often invoke selection and resulting evolution of
behavior. Also, phenotypic correlations between
conspecific males and females result from genetic
correlations. Little is known about the genetic basis of mating frequency in insects, but Pyle and
Gromko (1981) demonstrated that mating frequency in female D. melanogasterhas underlying
additive genetic variation, and Manning (1961,
1963) used artificial selection to enhance and also
to retard mating speed in D. melanogaster.Studies
of crickets and other Orthoptera have contributed
to an understanding of female mating frequency
in insects (Gwynne 1984; Sakaluk 1984, 1987; Sakaluk and Cade 1980, 1983; Simmons 1988), but
there are no data on the heritability of female repeated mating in this group. This study reports
on the frequency of female multiple mating in the
field cricket, Gryllusinteger, and the narrow sense
heritabilityunderlying this trait.
Methods
Data were collected between January1987 and February1988.
Laboratorycultures of G. integerwere established from specimens collected near Austin, Texas. This species is routinely
This content downloaded from 142.66.3.42 on Tue, 23 Jul 2013 16:57:03 PM
All use subject to JSTOR Terms and Conditions
74
referredto as G. integer, but this designation may be incorrect
(Smith and Cade 1987; Weissmannet al. 1980). Cultureswere
maintainedin 45 1 plastic garbage cans equipped with a 100 W
light and placed on a 12:12 h light: dark cycle at approximately
250 C. Water and Purina Cat Chow<' as a food source were
provided. Newly molted adult crickets were removed from the
cultures daily and isolated in individual containers that were
provided with water and food.
Four male G. integer were place in an observationchamber
(36 x 30 x 17 cm) 24 h before the start of observationseach day
to allow the males to acclimateand establishdominancehierarchies (Alexander 1961). The chamber contained food, water,
and an oviposition dish (500 ml) with moist vermiculite. The
temperaturein the laboratory was approximately250 C. Four,
individuallymarkedfemale G. integer were introducedinto each
observationchamber1 h into the light portion of the light cycle
(the laboratory was on a 12:12 h light:dark period). Females
had not mated previously and were between 4 and 11 days
of adult age when first observed. At this age most female G.
integer are receptive sexually. Observations were conducted
during the light portion of the light/dark cycle for 5 h each
day for 10 consecutive days. New males were used each day
so that females were never exposed to the same males for more
than one observation session. Data were collected in the light
to facilitate observations.Also, the highest frequencyof mating
behavior in G. integer in field populations is during daylight
hours (French and Cade 1987). Males typicallycourted females
throughout the observations and all females appearedto have
many opportunitiesto mate. Matings were recordedfor individual females if the female mounted the male and a spermatophore was attached. Female crickets often mount males, but
no spermatophoretransferoccurs (Sakaluk and Cade 1980).
Females were removed from the chambers and placed in
individual containers with food and moist vermiculitefor oviposition at the end of observations on each day. Females were
again placed in the chamber the next day. After the 10-day
observationperiod for a female, she was returnedto her oviposition container for 5 more days in order to collect additional
eggs. Juvenilecricketshatching from these eggs were the source
of individuals for the second set of observations on offspring.
Data from any females that died or that appeared unhealthy
during the 15 days were discarded. A total of 46 females were
observed in this manner.
Cultures from individual females were maintained and
adults removed as described previously. Ten daughters were
observed from each of the 46 females. Observationson daughters were conducted in an identical manner to those on the
parentalfemales.
The total number of times a female mated per day over
10 days was determinedfor mothersand daughters.The narrow
sense heritabilitywas calculated as the regression of the total
numberof matingsby daughterson the total numberof matings
by mothers. Since this method uses one parent, the narrow
sense heritability was estimated as 2 times the slope of the
regressionline, b (Falconer 1981).
The SE of the sampling variance of the regression coefficient, a was calculated as described in Falconer (1963, 1981)
and Zar (1984). The SE of the heritabilityestimate is 2 times
the SE of the regressioncoefficient.
Results
The number of times that individual females mated
in the parental generation is presented in Fig. 1.
Parental females mated 9.8 times on average (SD =
5
E
0
.0
E
0
5
10
15
20
25
30
Number of Matings
Fig. 1. The distributionof individual female G. integer mating
frequencyin the first generation
=7
. 55
II-
0
E
zi
TTTTT
1
5
TTIIF
10
15
Average Number of Matings
Fig. 2. The distribution of average female G. integer mating
frequencyfor familiesin the second generation
6.6, range= 1-30). The average number of matings
in each family of 10 females is presented in Fig. 2.
The average across the 46 families was 7.3 matings
per female (SD=3.4, range 1.9-16.2) and female
offspring mated from 0 to 26 times.
Bartlett'stest for homogeneity of varianceswas
performed. There was no significant difference between families in the variances of female mating
frequency (Z2=64.6, df= 45, P>0.05). A series of
Kolomogorov-Smirnoff tests on the offspring in
each family for goodness of fit to a normal distribution demonstrated deviations from normal in
only 6 of the 46 families. A linear regressionmodel
was therefore used.
The regression equation for the total number
of matings by daughters on the total number of
matings by mothers is y = 3.908 + 0.345 x, where
This content downloaded from 142.66.3.42 on Tue, 23 Jul 2013 16:57:03 PM
All use subject to JSTOR Terms and Conditions
75
3.908 is the y intercept and 0.345 (SE=0.14) is
the slope of the regression line. The slope was statistically significant (F = 35.5, P <0.0001). The narrow sense heritability is therefore estimated by
2 x 0.345 or 0.69 (SE = 0.29).
Discussion
Observations on female G. integer in the parental
population demonstrated a high degree of variation in the number of times females mated over
the 10 days. Some females mated only once, whereas one mated 30 times. These data are similar to
previous data for house crickets, Acheta domesticus, where females mated from 0 to 8 times with
an average frequency of 2.8 over 30 h of observations, and to data for G. integerfemales that mated
from 2 to 5 times in a single 6 h laboratory observation (Sakaluk and Cade 1980). There is also
much variation in female G. integer mating frequency in observations in large outdoor arenas
(Cade, in preparation).
This study demonstrated that mating frequency
in female G. integerhas underlyingadditive genetic
variation. The narrow sense heritability estimate
of 0.69 was statistically significant and indicates
that approximately 69% of the phenotypic variation in female G. integer mating frequency results
from genetic variation in loci with additive effects.
The SE of 0.29 indicates much variability around
this estimate. It is also apparent that environmental sources of variation influence female multiple
mating behavior. The narrow sense heritability estimate for G. integer multiple mating is within the
range reportedfor other behavioral and life history
traits (Cade 1984; Roff and Mousseau 1987). Estimates of narrow sense heritabilityfrom laboratory
studies are often inflated, however, over values for
the same trait in field populations. Higher estimates in the laboratory result from the reduced
environmentalvariation compared to field habitats
(Falconer 1981). No estimates are available of narrow sense heritabilities for female insect mating
frequency in field populations. In any case, the
estimate from this laboratory study suggests there
is ample additive genetic variation available for
selection on female mating frequencyin G. integer.
Although this study was not intended to examine the benefits of multiple mating, previous observations on crickets contribute to an understanding
of the function of female multiple mating behavior.
For example, in observations on house crickets,
female A. domesticus that mated twice produced
more offspring than singly mated females (Sakaluk
and Cade 1980). The difference resulted from the
failure of 12.5% of the singly mated females to
reproduce. A second mating in A. domesticusincreases the probability that a female is fertilized
and that offspring will be produced. But the high
level of multiple mating in female G. integer observed here cannot be explained by selection to
reduce the likelihood of failed inseminations.
Other benefits of female multiple mating in field
crickets may involve female consumption of spermatophores and spermatophylaxes(Sakaluk 1984,
1987), and transfer of egg development stimulants
(Bentur et al. 1977; Loher and Edson 1973). The
most detailed data on the function of repeated
mating in field crickets is from observations on
G. bimaculatus(Simmons 1988). Singly mated female G. bimaculatusdeplete the supply of spermatozoa in the spermatheca such that remating ensures an adequate supply of sperm. Recently mated
female G. bimaculatusalso readily consume spermatophores. Spermatophore consumption results
in increasedegg size and hatching success of progeny in this species.
It is also possible that female multiple mating
in G. integer is correlated with male multiple mating, but only if the costs to females are low. The
data on heritable variation presented here suggest
that artificial selection in the laboratory may alter
the frequency of female multiple mating. Artificial
selection experiments are necessary on female and
conspecific male multiple mating frequenciesto determine if multiple mating is a correlated genetic
trait between the sexes. Such data will add to an
understanding of the evolutionary significance of
repeated mating by female insects.
Acknowledgements.Funding was provided by a Natural
Sciences and EngineeringResearch Council of Canada operating grant (A6174). This study was from a portion of a thesis
submittedfor the M.Sc. degreefrom Brock University(B. Solymar). We thank K. Dixon, R. Morris,W. Ralph and S. Sakaluk
for comments on an earlierversion of the manuscript.
References
Alexander RD (1961) Aggressiveness,territoriality,and sexual
behavior in field crickets (Orthoptera: Gryllidae). Behaviour 17:130-233
Arnold SJ, HallidayT (1988) Multiplemating: naturalselection
is not evolution. Anim Behav 36:1547-1548
Bentur JS, Dakshayani K, Mathad SB (1977) Mating induced
oviposition and egg productionin the cricketsGryllusbimaculatus De Geer and PlebeiogryllusguttiventrisWalker. Z
Angew Entomol 84:129-135
Boriga G (1981) Mate selection in the fly, Scatophagastercoraria: female choice in a male-controlledsystem. Anim Behav 29:71-80
Cade WH (1984) Genetic variation underlyingsexual behavior
and reproduction.Am Zool 24:355-366
This content downloaded from 142.66.3.42 on Tue, 23 Jul 2013 16:57:03 PM
All use subject to JSTOR Terms and Conditions
76
Falconer DS (1963) Quantitativeinheritance.In: BurdetteWJ
(ed) Methodology in mammaliangenetics.Holden-Day, San
Francisco, pp 193-216
Falconer DS (1981) Introduction to quantitative genetics 2nd
edn. LongmannPress, New York, pp 340
French BW, Cade WH (1987) The timing of calling, movement
and mating in the field crickets Gryllusveletis, G. pennsylvanicusand G. integer.Behav Ecol Sociobiol 21:157-162
Gwynne DT (1984) Courtship feeding increases female reproductive success in bushcrickets.Nature 307:361-363
Halliday T, Arnold SJ (1987) Multiple mating by females: A
perspective from quantitative genetics. Anim Behav
35:939-941
Loher W, Edson K (1973) The effect of mating on egg production and releasein the cricket Teleogrylluscommodus.Entomol ExperAppl 16:483-490
Manning A (1961) The effects of artifical selection for mating
speed in Drosophilamelanogaster.Anim Behav 9:82-92
Manning A (1963) Selection for mating speed in Drosophila
melanogasterbased on the behaviour of one sex. Anim Behav 11:116-120
ParkerGA (1970) Spermcompetition and its evolutionaryconsequencesin the insects. Biol Rev 45:525-567
Pyle DW, Gromko MH (1978) Repeatedmating by female Drosophilamelanogaster:the adaptive significance.Experimentia 34:449-450
Pyle DW, Gromko MH (1981) Genetic basis for repeatedmating in Drosophilamelanogaster.Am Natur 117:133-146
Roff DA, Mousseau TA (1987) Quantitative genetics and fitness: Lessons from Drosophila.Heredity 58:103-118
Sakaluk SK (1984) Male crickets feed females to ensure complete sperm tranfer.Science 223:609-610
Sakaluk SK (1987) Reproductive behaviour of the decorated
cricket,Gryllodessupplicans(Orthoptera:Gryllidae):calling
schedules, spatial distribution and mating. Behaviour
100:202-225
Sakaluk SK, Belwood JJ (1984) Gecko phonotaxis to cricket
calling song: A case of satellite predation. Anim Behav
32:659-662
Sakaluk SK, Cade WH (1980) Female mating frequency and
progeny production in singly and doubly mated house and
field crickets. Can J Zool 58:404-411
Sakaluk SK, Cade WH (1983) The adaptive significance of
female multiple mating in house and field crickets. In:
Gwynne DT, Morris GK (eds) Orthopteramating systems:
sexual selection in a diverse group of insects. Westview
Press, Boulder, pp 319-336
ShermanPW, WestneatDF (1988) Multiplemating and quantitative genetics. Anim Behav 36:1545-1547
Simmons LW (1988) The contribution of multiple mating and
spermatophore consumption to the lifetime reproductive
success of female field crickets (Gryllusbimaculatus).Ecol
Entomol 13:57-69
SivinskiJ (1980) Sexualselectionand insect sperm.Fla Entomol
63:99-111
Smith CJ, Cade WH (1987) Song characteristicsand fertility
in hydridization experiments on the field crickets, Gryllus
integerand G. rubens.Can J Zool 65:2390-2394
ThornhillR (1976) Sexual selection and nuptial feeding behavior in Bittacus apicalis (Insecta: Mecoptera). Am Nat
110:529-548
Thornhill R, Alcock J (1983) The evolution of insect mating
systems. HarvardUniv Press, Cambridge,pp 547
Walker WF (1980) Sperm utilization strategies in non-social
insects. Am Nat 115:780-799
Weissman DB, Rentz DCF, Alexander RD, Loher W (1980)
Field crickets (Gryllusand Acheta) of California and Baja
California, Mexico (Orthoptera: Gryllidae: Gryllinae).
Trans Am Entomol Soc 106:327-356
Wing SR (1988) Cost of mating for female insects: risk of predation in Photinus collustrans (Coleoptera: Lampyridae).
Am Nat 131:139-142
Zar JH (1984) Biostatisticalanalysis.Prentice-Hall,New Jersey,
pp 718
This content downloaded from 142.66.3.42 on Tue, 23 Jul 2013 16:57:03 PM
All use subject to JSTOR Terms and Conditions