spatio-temporal variation in mating success of female bagworms

SPEC IAL ISSUE : FEMALE MAT ING FA ILURES IN INSECTS

Spatio-temporal variation in mating success of femalebagwormsMarc Rhainds*Natural Resources Canada, Canadian Forest Service – Atlantic Forestry Centre, PO Box 4000, Fredericton, New Brunswick,

Canada E3B 5P7

Accepted: 19 December 2011

Key words: Lepidoptera, reproductive isolation, operational sex ratio, female mating failure, Thyri-

dopteryx ephemeraeformis, Psychidae

Abstract The study investigated spatio-temporal variation in the mating success of female bagworms, Thyri-

dopteryx ephemeraeformis Haworth (Lepidoptera: Psychidae), across a broad latitudinal range in

Indiana, USA, between 2007 and 2009. A series of interconnected equations based on estimates of

demographic parameters at different intervals was used to derive the punctual sex ratio and female

mating success early and late in the season. Both the mating success of females and the relative abun-

dance of bagworms declined with latitude, which provides indirect support to the mate encounter

Allee hypothesis. However, the late emergence of females at northern locations combined with the

consistently low mating success of late-emerging females suggests that the impact of latitude on mat-

ing probability is indirectly mediated by emergence time. A variable level of protandry was observed

each year, and the low ratio of males per female late in the season was associated with low female mat-

ing success. The reduced level of activity of males at temperatures below 18 �C may also account for

the low mating probability of late-emerging females. The weak, inconsistent effect of local variation

in sex ratio on female mating success suggests that males commonly disperse from their natal patch, a

behavior that may have evolved to reduce inbreeding in local populations of bagworms. Altogether,

these results suggest that temporal variation in sex ratio has a greater impact on the mating success of

female bagworms than spatial variation in sex ratio.

Introduction

Variation in the density, sex ratio, and seasonality of insect

populations in fragmented landscapes influences the mat-

ing success of females (Tobin et al., 2007; Rhainds &

Fagan, 2010). The operational sex ratio is a strong determi-

nant of mating success and a low abundance of males is

usually associated with female mating failures (Higgins,

2000; del Castillo & Nunez-Farfan, 2002; Muralimohan &

Srinivasa, 2010). The influence of sex ratio on mating fail-

ures is modulated by two distinct, but not exclusive mech-

anisms, reproductive isolation of females in space or time

(Calabrese & Fagan, 2004; Robinet et al., 2007). Spatial

isolation refers to extreme bias of sex ratio in local popu-

lations, whereas temporal isolation refers to disjunction in

the emergence pattern of males or females (protandry or

protogyny). Spatial variation in phenology of adult emer-

gence has been documented in many insects (Kingsolver,

1989; Weiss et al., 1993; Rooney et al., 1996; Fielding et al.,

1999), but discriminating between the effects of spatial or

temporal reproductive isolation on mating failures is chal-

lenging due to logistic difficulties in tracking down lifetime

events for small, mobile females (Rhainds, 2010).

Insect species with flightless females provide model sys-

tems to study mating success, because in situ post-mortem

dissections can be used to determine whether a female has

mated during her life or not, and the probability of mating

can be related directly to the environment where the

female is located (Rhainds, 2010). Under a scenario where

both males and females have limited dispersal capacity, the

mating success of females would be expected to coincide

spatially with the local abundance of males, as is the case in

resident mating aggregations (Masters et al., 1994; Nagel-

kerke & Sabelis, 1998). In a majority of species with flight-

less females, however, males are winged and fully capable*Correspondence: E-mail: [email protected]

� 2012 Her Majesty the Queen in Right of Canada Entomologia Experimentalis et Applicata 1–7, 2012

Entomologia Experimentalis et Applicata � 2012 The Netherlands Entomological Society 1

DOI: 10.1111/j.1570-7458.2012.01224.x

of flight (Roff, 1990; Wagner & Liebherr, 1992). The mat-

ing success of females may thus be independent of the local

sex ratio under circumstances where male dispersal

between populations is prevalent (Rhainds et al., 2008), in

which case, temporal variation in sex ratio induced by

protandry may have a greater influence on female mating

success than the local abundance of males. Unfortunately,

the rate of dispersal by winged males in species with flight-

less females has not been thoroughly investigated. Pre-

reproductive dispersal of adults has evolved, in part, to

reduce the potentially high fitness cost of inbreeding (Mo-

tro, 1991; Gandon, 1999; Hirota, 2004), and the presum-

ably high level of genetic relatedness in local populations

with flightless females (Rhainds et al., 2009) may have

selected for a high incidence of dispersal among males.

Empirical investigations on the rate and range of dispersal

in field populations of insects are notoriously difficult to

conduct or even interpret (Prugnolle & de Meeus, 2002).

Molecular markers are a potentially useful tool to monitor

the dispersal of males between populations (Behura,

2006), but these techniques have been applied to few spe-

cies with flightless females (Grapputo et al., 2005).

The incidence of male dispersal can be assessed indi-

rectly by comparing the mating success of sessile females

relative to the local abundance and sex ratio in discrete

(isolated) populations among early and late-emerging

females. This approach is elaborated with the bagworm,

Thyridopteryx ephemeraeformis Haworth (Lepidoptera:

Psychidae), a univoltine species with a wide distribution in

the USA and a broad range of host plants (Rhainds et al.,

2009). Shortly after hatching in early June, neonate bag-

worms construct a self-enclosing bag made of silk and

plant material that they enlarge through larval develop-

ment. The neonates either balloon on surrounding host

plants before feeding, or remain on the same plant where

they emerged. The larvae tightly attach their bags to the

host plant prior to pupation and emerge as adults 2–4

weeks later in the fall. Neotenic females are flightless and

reproduce within their bag, whereas males are winged and

capable of flight. Females attract mates by releasing phero-

mone-impregnated scales in the lower segment of their

bag. For copulation, the male inserts his extensible abdo-

men inside the bag and pupal case of the female to reach

her genitalia. Shortly after mating, the female oviposits in

her pupal case and then drops on the ground to die; as in

other bagworm species, a large proportion of females do

not mate as adults. The eggs overwinter within the pupal

case of their mother, and hatch synchronously in the spring.

A recent study has revealed a strong latitudinal decline

in female mating success, to such an extent that at some

northern locations, all females fail to mate during their life-

time (Rhainds & Fagan, 2010). However, it remains

unclear whether this can be attributed to latitude per se or

to other factors that co-vary with latitude, for example,

population density, sex ratio, or timing of adult emer-

gence. A mechanistic approach derived from field data is

developed to estimate parameters that affect the mating

success of female bagworms and determine whether mat-

ing failures are primarily caused by reproductive isolation

in space or time.

Materials and methods

Demographic assessment

Bags that were collected at different sites through the study

were cut open longitudinally to reveal their content. Indi-

viduals that had died during the larval or pupal stages were

discarded from analysis. The remaining individuals were

classified as pupa (pm for males, pf for females) or adult

(em or ef for emerged males and females). Adult females

were further classified as either mated-dead (inseminated

female, or if), unmated-dead (uf), or live calling (cf); for

analysis, calling females were regrouped with female pupae

because their subsequent mating success could not be pre-

dicted. The criteria used to categorize the individuals

include the distinct morphological shape of male and

female pupa, the presence of an empty pupal case protrud-

ing from the anterior segment of the bag (em), the pres-

ence of pheromone-impregnated yellow scales inside the

lower portion of the bag combined with a split of the ante-

rior segment of the pupal case (ef), the presence of eggs

inside the pupal case (if), the absence of eggs inside a bag

containing a dead female (uf), and the presence of a live

female inside the pupal case (cf) (Table 1 in Rhainds et al.,

2008). The following parameters were estimated for the

different sites: proportion of adult emergence (EM and

EF), mating success of females (MS), and sex ratio

(RATIO):

EM ¼ em=ðpmþ emÞ; ð1Þ

EF ¼ ðif þ ufÞ=ðif þ uf þ cf þ pfÞ; ð2Þ

MS ¼ if=ðif þ ufÞ; and ð3Þ

RATIO ¼ em=ef : ð4Þ

Estimates of mating success obtained after all adults had

emerged are indicative of the overall proportion of mated

2 Rhainds

females (MScumul), because EM = EF = 1 at the end of the

reproductive season. Estimates obtained during the course

of the reproductive season (before all females have com-

pleted reproductive activity) represent the mating success

of females up to the time of sampling (MSearly), which cor-

responds to given proportions of emerged females (EFearly)

and males (EMearly). The mating success of females that

emerged late in the season, between two sampling inter-

vals, was estimated by taking into account the proportions

of early emerging females and of mated females at different

intervals:

MScumul ¼ if cumul=ðif cumul þ uf cumulÞ; ð5Þ

MSearly ¼ ifearly=ðif early þ uf earlyÞ; and ð6Þ

MSlate ¼ ½MScumul � ðEFearly �MSearlyÞ�=ð1� EFearlyÞ:ð7Þ

For analysis, values of MSlate at different sites were con-

strained between 0 and 1. Variation in sex ratio over time

can be assessed using the total number of males and

females sampled at a given site (M and F) and the propor-

tion of emerged adults early in the season as follows:

RATIOearly ¼ emearly=efearly; and ð8Þ

RATIOlate ¼ ½M� ð1� EMearlyÞ�=½F� ð1� EFearlyÞ�:ð9Þ

Experimental sites consisted of an individual plant or a

cluster of plants that was >50 m away from other plants

infested with bagworms. Only sites with a relatively high

density of bagworms were sampled during the study

because estimates of proportional data or ratios are subject

to a high level of imprecision when the sample size is small;

hence, the data cannot be used to evaluate the effect of

small-scale variation in population density on female mat-

ing success.

Sampling procedure for the 2007 generation of bagworms

Twenty-three sites were sampled through the summer of

2007 in central Indiana, USA (40.0–40.5�N, 86.4–87.4�W)

(Rhainds et al., 2008). Bagworms collected at different

sites were dissected and classified as described above. The

variables were analyzed at all locations for two time

periods, on 17 September, when approximately half the

females had emerged, and on 1 October when most

(>97%) of adults had emerged. The individuals that had

not reached the adult stage by 1 October were deleted from

analysis.


A total of 27 sites (Figure 1) were sampled in Indiana

twice, the first time during the period of adult emergence

between 3 and 16 of October 2008, and the second time in

March 2009, after all individuals had completed reproduc-

tive activity (EM = EF = 1). The study sites were selected

by driving through Indiana and inspecting junipers or

arborvitae for the presence of bagworms; between 50 and

200 bags were collected at each site and time period. Each

bag was dissected and the individuals were classified as

described above. The abundance of males was not assessed

during the second sampling period because the empty

pupal case protruding from the bag of emerged males had

generally fallen on the ground by the end of the winter.

The sex ratio of early and late-emerging adults was thus

evaluated using sampling estimates based only on the first

sampling assessment in October.


Forty-six sites (Figure 1) were sampled repeatedly through

the entire period of adult emergence (10 August–

15 November) at an interval of 6–10 days between sam-

pling periods (Rhainds & Fagan, 2010). For each site, a

logistic regression model of the form y = e(bo + b1 x) ⁄[1 + e (bo + b1 x)] was used to evaluate the proportion of

post-reproductive females (y) as a function of time (x,

expressed as Julian date) and to derive the date that corre-

sponded to 50% post-reproductive females (EF = 0.5).

Logistic models of male emergence were also used to eval-

uate EM at the time when EF = 0.5, to calculate the ratio

of males per female early in the season. For analysis, the

data were classified in two periods (early season and

cumulative) for values of EF smaller or greater than 0.5. As

Figure 1 Spatial location of sites sampled in Indiana to determine

the mating success of female Thyridopteryx ephemeraeformis in

2008 and 2009.

Mating success of female bagworms 3

EF usually exceeded 90% during the subsequent sampling

period after EF = 0.5, estimates of female mating success

based on the second half of the emergence cycle provided

reasonably good approximations of MScumul.

Longevity of adults

Pupae collected in the field in September 2009 were indi-

vidually enclosed in small plastic cups (Solo cups) and

maintained at ambient conditions in the laboratory. The

individuals were monitored 4–5 times per day, at intervals

of 3–8 h, to determine the timing of adult emergence and

mortality. The criteria used to determine emergence for

males were the presence of a live moth that had emerged

from a dehisced pupal case, and for females, the presence

of a split in the anterior segment of the pupal case and the

shedding of pheromone-impregnated scales outside of the

pupal case. Mortality of males and females was indicated

when individuals did not react to a gentle tweaking with a

forceps; for females, this was done after the individual had

left her pupal case. The longevity of females that remained

inside their pupal case until death could not be assessed. In

total, longevity was assessed for 84 males and 186 females.

Statistical analysis

Statistical analyses were conducted using the SAS program

(SAS Institute, Cary, NC, USA). Longitude was excluded

from analysis because it has a considerably weaker effect

on the demography of bagworms than latitude (Table 2 in

Rhainds & Fagan, 2010). For analysis, the sites were

regrouped in four 0.5� latitudinal bins from LAT = 1 for

sites <40�N to LAT = 4 for sites >41�N. A generalized lin-

ear model including all two-way interaction terms was

used to evaluate (1) RATIO as a function of LAT and

TIME (early and late season) and (2) the estimated pro-

portion of mated females (MSearly and MSlate) as a function

of RATIO, LAT, and TIME; a backward stepwise approach

was used in which the least significant variables were

deleted one at a time until only significant parameters

remained in the final model. The analysis in 2007 did not

include LAT because all sites were located at one latitudi-

nal bin. Data were subjected to � (ratio of males per

female) and arcsine (proportion of emerged adults and

mated females) transformations to reduce heteroscedastic-

ity of variance.

Results

2007 generation of bagworms

On average, 50% of females had emerged during the first

sampling period, of which 96% were mated. The propor-

tion of emerged adults did not differ for males and females

(F1,42 = 0.71, P = 0.40), but the ratio of males per female

was marginally lower early in the season than late in the

season (F1,44 = 3.57, P = 0.40). The mating success of

females declined over time (F1,44 = 17.15, P = 0.0002);

neither sex ratio nor the interaction sex ratio*time influ-

enced mating probability. The mating success of late-

emerging females was independent of the local sex ratio

(r2 = 0.033, P = 0.41) (Figure 2); the relation could not

be evaluated for early emerging females, because a vast

majority of them were mated (Table 1).


On average, 63% of females had completed reproductive

activity during the first sampling period, of which 83%

were mated. The proportion of emerged adults declined

with latitude for females (r2 = 0.215, P = 0.015) but not

for males (r2 = 0.045, P = 0.29); males emerged more or

less in synchrony with females at latitudes below 41�N and

before females at higher latitudes (Table 1). The sex ratio

was influenced by the interaction time*latitude (F = 3.85,

d.f. = 1,51, P = 0.028), which was due to the similar abun-

dance of both sexes early and late in the season at latitudes

<40�N (Table 1). The punctual mating success of females

was influenced by the timing of emergence (F1,52 = 41.99,

P<0.0001), as indicated by the consistently higher proba-

bility of mating of early emerging females (Table 1). The

sex ratio at different locations had no effect on the mating

success of early (r2 = 0.019, P = 0.49) or late (r2 = 0.019,

P = 0.50) emerging females (Figure 2).


The date corresponding to 50% of post-reproductive

females varied between 11 August and 15 November and

increased with latitude (r2 = 0.445, P<0.0001); the late

emergence of females was most striking above 41�N

(Table 1). The relationship between latitude and the pro-

portion of emerged males was marginally insignificant

Figure 2 Relationship between the ratio of males per female and

the mating probability of early and late-emerging female Thyrido-

pteryx ephemeraeformis. The relationship was not evaluated in

early season in 2007 because the vast majority of females were

mated.

4 Rhainds

(r2 = 0.099, P = 0.055). At the time corresponding to

EF = 0.5, the proportion of emerged males averaged

>70% at all latitudinal bins. The ratio of males per female

declined with latitude (F1,87 = 11.49, P = 0.001) and was

higher early in the season (F1,87 = 13.69, P = 0.0004)

(Table 1). The punctual mating success of females

declined with latitude (F1,87 = 67.96, P<0.0001); the

significant interaction time*latitude (F1,87 = 15.76,

P<0.0001) was due to the similar probability of mating

among early and late-emerging females at locations south

of 40�N, compared with the considerably lower probability

of mating for late-emerging females at locations north of

41�N (Table 1). The mating success of females increased

with the ratio of males per female early in the season

(r2 = 0.109, P = 0.027), but the effect was marginally

insignificant late in the season (r2 = 0.056, P = 0.12)

(Figure 2).

Longevity of adults

Males lived 3–84 h, and females lived 24–337 h. The med-

ian longevity was 1.5 days for males and 6.5 days for

females (Figure 3).

Discussion

The abundance of T. ephemeraeformis, expressed in terms

of number or proportion of infested plants, declines from

south to north in Indiana, which suggests that latitude has

a direct effect on female mating success through variation

in population density (Rhainds & Fagan, 2010). The link

between latitude, population density, and mating proba-

bility, provides indirect support to the Allee effect hypoth-

esis on a large scale, especially because low rates of

reproduction have been associated with extinction of local

populations and the geographic range limit of bagworms

in Indiana meshes spatially with the area where females

experience low mating success (Rhainds & Fagan, 2010).

The late emergence of females at northern locations com-

bined with the consistently low mating success of females

that emerge late in the season suggests that the impact of

latitude on mating probability is indirectly mediated by

emergence time. In 2008, for example, only emergence

time (and not latitude per se) had a significant effect on

the mating success of females (Table 1). The decline in

cumulative mating success of females was due to the late

emergence of females at northern locations rather than a

direct effect of latitude on mating probability. The mating

success of females in 2009 was impacted by latitude,

although the significant interaction, time*latitude, indi-

cated that the strength of the relationship varied for

females emerging early or late in the season.

Low mating success of late-emerging females has been

predicted by theoretic models (Calabrese & Fagan, 2004;

Robinet et al., 2007), and the hypothesis was validated in

Table 1 Demographic parameters related to the mating success of female Thyridopteryx ephemeraeformis at different locations in Indiana

Year Latitude EF EM RATIOcumul RATIOearly RATIOlate MScumul MSearly MSlate

2007 40.0–40.5 0.50 ± 0.06 0.58 ± 0.08 0.75 ± 0.20 1.15 ± 0.30 0.41 ± 0.10 0.86 ± 0.03 0.96 ± 0.02 0.67 ± 0.08

2008 <40.0 0.81 ± 0.01 0.79 ± 0.06 0.87 ± 0.14 0.84 ± 0.15 0.97 ± 0.27 0.81 ± 0.03 0.92 ± 0.05 0.33 ± 0.13

40.0–40.5 0.69 ± 0.06 0.81 ± 0.05 0.50 ± 0.13 0.66 ± 0.23 0.36 ± 0.14 0.67 ± 0.08 0.86 ± 0.04 0.33 ± 0.13

40.5–41.0 0.54 ± 0.08 0.64 ± 0.11 0.55 ± 0.12 0.64 ± 0.16 0.32 ± 0.06 0.62 ± 0.07 0.87 ± 0.03 0.26 ± 0.22

>41.0 0.49 ± 0.09 0.73 ± 0.09 0.83 ± 0.56 1.21 ± 0.81 0.31 ± 0.15 0.43 ± 0.15 0.57 ± 0.20 0.17 ± 0.15

2009 <40.0 0.5 (273 ± 3) 0.86 ± 0.06 0.96 ± 0.17 1.31 ± 0.24 0.58 ± 0.15 0.85 ± 0.05 0.93 ± 0.03 0.78 ± 0.07

40.0–40.5 0.5 (277 ± 4) 0.81 ± 0.13 0.59 ± 0.08 0.83 ± 0.10 0.36 ± 0.10 0.73 ± 0.11 0.85 ± 0.07 0.64 ± 0.14

40.5–41.0 0.5 (275 ± 3) 0.73 ± 0.06 1.70 ± 1.12 1.91 ± 0.91 1.49 ± 0.37 0.47 ± 0.05 0.59 ± 0.17 0.34 ± 0.13

>41.0 0.5 (302 ± 3) 0.70 ± 0.04 0.22 ± 0.06 0.30 ± 0.11 0.14 ± 0.04 0.17 ± 0.04 0.43 ± 0.11 0.09 ± 0.06

EF and EM = proportion of, respectively, emerged females and males early in the season. RATIOcumul ⁄ early ⁄ late = ratio of males per female

at different time intervals. MScumul ⁄ early ⁄ late = proportion of mated females at different time intervals. The parameters were estimated

using equations 1–9 in Materials and methods. The values in parentheses in 2009 indicate the Julian dates corresponding to EF = 0.5 as

estimated by logistic regression model.

Figure 3 Lifespan of male and female Thyridopteryx ephemerae-

formis estimated under laboratory conditions.


some insects (Higgins, 2000; Calabrese et al., 2008; Mural-

imohan & Srinivasa, 2010). Male bagworms emerged

before females and protandry resulted in a lower ratio of

males per female late in the season, which was associated

with highly significant decline in mating probability over

time (Table 1). The reduced level of activity of short-lived

males when the temperature is below 18 �C (Figure 3;

Morden & Waldbauer, 1971) may also account for the low

mating probability of late-emerging females.

Despite the advantage of flight for resource location,

predator avoidance and dispersal, many orders of insect

include species with flightless females. The loss or reduc-

tion of wings in females has probably evolved in part as a

physiologic adaptation to increase reproductive output

(Roff, 1986; Zera & Denno, 1997), whereas males may have

retained their flight capacity to facilitate mate location

(Roff, 1990). Local populations of bagworms may be char-

acterized by a high level of genetic relatedness, because the

larval progeny of females commonly do not disperse from

the host plant where they emerged (Rhainds et al., 2009),

and pre-reproductive dispersal of males may thus have

evolved as a strategy to reduce inbreeding. The weak rela-

tionship between female mating success and the local abun-

dance of males (Figure 2) is consistent with the hypothesis

that males regularly disperse from their natal patch.

In conclusion, temporal variation in sex ratio appears to

have a greater impact on the mating success of female

T. ephemeraeformis than spatial variation in sex ratio. The

mechanistic approach derived in this study (equations

1–9) may provide a useful tool to evaluate spatio-temporal

variation in mating success for other insect species, and it

illustrates the importance of empirical data in substantiat-

ing ecological theory (Rigler, 1982).

Acknowledgments

I thank W.F. Fagan, G. Gries, H. Lynch, and C. Sadof for

their support. X. Fauvergues, B. Roitberg, S. Matter, and

one anonymous reviewer provided useful comments on an

early version of the manuscript.

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