Behavioral Ecology Vol. 13 No. 4: 519-525
© 2002 International Society for Behavioral Ecology
The evolution of soldier reproduction in social thrips
a School of Biological Sciences, Flinders University of South Australia, GPO Box 2100, Adelaide, SA 5001, Australia b Laboratory of Insect Resources, Tokyo University of Agriculture, 1737 Funako, Atsugi-shi, Kanagawa 243-0034, Japan c CSIRO Entomology, GPO Box 1700 Canberra, ACT 2601, Australia d Department of Biosciences and Behavioural Ecology Research Group, Simon Fraser University, Burnaby, BC V5A 1S6, Canada
Address correspondence to: T.W. Chapman. E-mail: tom.chapman{at}flinders.edu.au .
Received 16 May 2001; revised 5 October 2001; accepted 15 October 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We estimated the degree of reproductive differentiation between foundresses and soldiers in multiple populations of five species of haplodiploid Australian gall-forming thrips using microsatellite data, ovarian dissections, and census data. Microsatellite-based species estimates of average per capita reproductive output of soldiers relative to the foundresses ranged from 0.005 to 0.64, and dissection and census-based estimates ranged from 0.17 to 1.1. Mapping of these estimates onto a phylogeny showed that levels of soldier reproduction were apparently higher in three basal lineages than in two more derived lineages. We infer from this phylogenetic pattern that soldier morphology and behavior of thrips evolved in the presence of substantial levels of soldier reproduction. This pattern of evolutionary change is similar to that proposed for the origin of soldiers in aphids and termites, but it differs from the scenario proposed for the origin of workers in Hymenoptera, within which helping and strong reproductive division of labor apparently evolved before morphological differentiation. We suggest that this difference in evolutionary routes to eusociality between taxa with soldiers and taxa with foraging workers was driven by a weaker trade-off between helping and reproducing, and a greater ability of the helpers to withstand reproductive domination, in taxa with soldiers. This is the first study to analyze the social-evolutionary trajectories of reproductive, behavioral, and morphological differentiation in the context of a species-level phylogeny.
Key words: castes, inbreeding, microsatellites, soldiers, thrips.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Reproduction by helpers is a common feature of social insects that is closely linked to the evolution of many colony characteristics, including dominance behavior, egg cannibalism, brood destruction, matricide, reduced efficiency, and rarity of physical castes among helpers (Bourke, 1988
;
Strassmann, 1988;
Woyciechowski, 1989). Indeed,
Trivers and Hare (1976)
suggested that production of sons by incipient helpers facilitated the origin
of eusociality in haplodiploids, and several theoretical studies have
substantiated a potential role for parthenogenic male production to increase
the ease of helper evolution (Aoki and
Moody, 1981; Bartz,
1982; Crozier and Pamilo,
1996; Iwasa, 1981;
Pamilo, 1984,
1991). Despite the importance
of helper reproduction for the origin and evolution of eusociality, its
prevalence and coevolution with other social traits have yet to be analyzed in
an explictly phylogenetic context.
We believe that analysis of soldier reproduction in the social,
haplodiploid gall-forming thrips of Australia holds particular promise for
understanding the origin and evolution of helper reproduction because (1)
soldier mating and egg laying appear to be prominent features of social thrips
(Crespi, 1992a; Kranz et al.,
1999,
2001a,
b) and (2) a well-supported
phylogeny for the gall-forming thrips of Australia exists
(Crespi et al., 1998;
Morris, 2000), allowing
inference of the evolutionary history of soldier reproduction. In this study
we estimated the extent of soldier reproduction in multiple populations of
five species of gall-forming thrips in Australia. We estimated levels of
soldier reproduction using two approaches. First, we used microsatellite
genetic markers and a population genetic model described below. Second, we
used ovarian dissection and colony census data. Here we evaluate the resulting
multispecies pattern of soldier reproduction, in a phylogenetic context, and
we discuss the role that soldier reproduction may have played in the origin
and evolution of eusociality in thrips and other insects.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study populations and natural history
The gall-forming thrips of Australia are composed of three genera: Onychothrips, Kladothrips, and Oncothrips, with eusocial species occurring in the latter two genera (Crespi et al., 1998
).
Gall-forming thrips are mostly restricted to the arid and semiarid zones of
Australia, and each thrips species is associated with specific Acacia
host tree species (Crespi and Mound,
1997). A colony is initiated by a single female (or, in some
species, a single female with a male) who induces gall formation on a growing
phyllode of a host Acacia tree. En-closed within the gall, the
founding female lays her eggs. The first individuals of a foundress's brood to
eclose are the gall-bound soldiers, which are morphologically and behaviorally
specialized for defense, with reduced wings and enlarged forelegs
(Crespi, 1992a). The soldiers
include both sexes (Crespi,
1992a,b;
Crespi and Mound, 1997;
Crespi et al., 1997). The
foundress's life span overlaps with the soldiers, but she dies before the
dispersing brood reaches the adult stage. Studies show that female soldiers
are often inseminated provided there were male soldiers in the gall
(Kranz et al., 2001b).
Demographic collection data indicates that if soldiers reproduce, they could
only be producing dispersers (Crespi,
1992a,b,
unpublished data).
In this article, we use the term "helper" to refer to both
workers and soldiers. As defined here, workers are individuals specialized for
foraging, brood rearing, or both, and soldiers are morphologically and
behaviorally specialized to defend their colony. A group of soldiers
represents a caste, a defining characteristic of eusociality, only if there is
a reproductive division of labor (Crespi
and Yanega, 1995).
Collection data for the five gall-forming species with soldiers in our
study are listed in Appendix A. At each collection site, galls were taken from
a stand of several trees in close proximity, such that population subdivision
above the level of the individual gall is unlikely to contribute to any
deviations from Hardy-Weinberg expectations
(Blows and Schwarz, 1991;
Pamilo, 1985). Collections
used in genetic analysis for four species, Kladothrips hamiltoni,
Oncothrips habrus, Oncothrips morrisi, and Oncothrips
waterhousei contained a foundress female, adult soldiers, first- and
second-instar larvae, and some eggs. The collections of Oncothrips
tepperi used in genetic analysis contain soldiers and adult dispersing
brood.
Microsatellite markers
Genetic data were gathered using microsatellite markers developed
specifically for gall-forming thrips. Data collections were made for
foundresses and soldiers for four species: K. hamiltoni, O. habrus, O.
waterhousei, and O. morrisi. For O. tepperi genotype
data were collected for all soldiers in the two populations sampled, and a 25%
random sample of the adult female dispersing brood (males are hemizygous and
therefore are not useful for estimating homozygosity levels; see model below)
from each gall in our collections was also genotyped. The preparation of
samples, the determination of microsatellite genotypes, and primer sequences
used in this study are reported in Chapman et al.
(2000). A summary of loci used
and number of alleles found in each case is presented in the Appendix.
Model for estimating soldier production of female dispersers
Dispersing brood can be produced in the gall of a thrips species with
soldiers in two ways: (1) the foundress produces soldiers and dispersers, and
(2) the foundress produces soldiers and the soldiers produce all or some of
the dispersers. If the foundress produces all of the female dispersers, then
the inbreeding coefficient (FIS) is expected to
be identical for the soldiers and the dispersers (i.e.,
FIS measured using soldier genotypes is equal to
FIS measured using disperser genotypes). If,
however, soldiers produce all the dispersing females (via sib-mating), then
the inbreeding estimate using disperser genotypes is expected to increase over
that of the soldiers, and the level of increase expected can be determined
using the inbreeding recursion equation for full-sib mating:
FIS(generation t+1) = 
+
FIS(t) +
FIS(t-1)
(Laidlaw and Page, 1986). When
soldiers produce only a proportion of dispersing females, the inbreeding
coefficient measured in the dispersing generation (female dispersers produced
by the foundress or by soldiers) increases proportionately to the extent that
soldiers produce female dispersers. Thus, the inbreeding coefficient of the
current generation of dispersing females
[FIS(D)] can be estimated using the
inbreeding coefficient of the soliders
[FIS(S)], the previous generation of
dispersers [FIS(D-1)], soldier-produced
female dispersers (spfd), and the inbreeding recursion equation for
full-sibling mating [ +
FIS(S) +
FIS(D-1)] in the following equation:
 | (1) |
When soldiers produce none of the female dispersers (spfd = 0),
the above equation reduces to FIS(D) =
FIS(S) as expected. When soldiers
produce all the female dispersers (spfd = 1), the inbreeding
coefficient of the dispersers increases by the increment predicted by the
recursion equation for one generation of full-sib mating
[FIS(D) = +
FIS(S) +
FIS(D-1)].
Equation 1 assumes that soldier females mate only with siblings. This
assumption is reasonable given that galls are initiated by a single female and
gall membership appears to be stable
(Chapman and Crespi, 1998).
Genetic data from two generations of gall initiation would be difficult to
obtain for the gall-forming thrips. Equation 1 can be simplified for a
single-season collection of galls by assuming
FIS(D) is at equilibrium such that
FIS(D) =
FIS(D-1) and solving Equation 1 for
spfd:
 | (2) |
).
Ovarian dissection and census data collections for estimating soldier
production of female and male dispersers
For the collections K. hamiltoni (census), O. morrisi
(census), O. waterhousei (census), and O. habrus (census),
foundresses and a sample of soldiers from each gall were dissected to
determine the number of chorionated oocytes in each morph (see
Kranz et al., 1999). Oocytes
that are chorinated have hexagonal reticulation that is characteristic of all
eggs in the tubuliferan suborder and can be viewed with a light microscope.
The number of soldiers dissected varies between species analyzed, but ranges
from 71 to 224. For these estimates we assume that fecundities of foundresses
and soldiers are positively correlated with the number of chorionated oocytes.
Chorionated oocyte counts therefore represent the relative contribution of the
foundress and soldiers to the dispersing brood. We dissected both morphs when
they were likely producing eggs destined to be dispersers (i.e., when gall
brood size was larger than the maximum number of soldiers expected for a
species). For O. tepperi (census), regressions of the number of
dispersers on the number of female soldiers were conducted to estimate the
proportion of the disperser brood that was produced by the foundress (the
y intercept). The number and sex ratio of soldiers and dispersers
were ascertained from multiple gall collections throughout the life cycle of
each species.
Statistical analysis
Inbreeding calculations using microsatellite data were conducted using the
computer program Relatedness 4.2c (Goodnight KF, Rice University). Formulae
used in this computer program are described in Queller and Goodnight
(1989).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Microsatellite estimates of the proportion of female dispersers produced by soldiers
Inbreeding coefficients in soldiers and dispersers were estimated for all five species (Table 1). Inbreeding estimates ranged from 0.0 to 0.8, with the highest values found for K. hamiltoni. Inbreeding values for dispersers were higher than those of soldiers in all populations, and estimates of the proportion of soldier-produced female dispersers (spfd) ranged from 5% to 85% (Table 1).
|
Soldier per capita production of female dispersers (spfd/number of female soldiers) relative to the foundress contribution (1 — spfd) ranged from 0.005 to 0.64 (Table 1). Per capita estimates were also calculated under the assumption that the soldiers produce all of the dispersing males, and these per capita estimates ranged from 0.052 to 0.70 (Table 1).
Ovarian dissection and census data estimates of soldier production of
female and male dispersers
The proportion of dispersing males and females produced by soldiers was
estimated for all five species and ranged from 40% to 96%
(Table 1). Estimates of soldier
reproduction based on these data were consistently higher than estimates, for
the same species, using microsatellite data
(Table 1). The broad pattern
seen in the genetic data of relatively high (O. waterhousei, O.
morrisi, and K. hamiltoni) and low (O. habrus and
O. tepperi) soldier reproduction is also apparent from these
estimates.
Soldier per capita production of dispersers relative to the foundress contribution ranged from 0.07 to 1.1 (Table 1). These estimates were generally higher than per capita estimates using microsatellite data for a given species.
Production of male dispersers by soldiers in the population O. tepperi 2 (the only species for which we had both completely developed broods and microsatellite data) is supported by a regression of number of male dispersers on number of female soldiers present in the gall (y = 1.45 + 2.26, r2 =.61, p =.0002). Soldiers in this population are each producing approximately 4-5 (4.7) disperser males (6.95 disperser males per colony minus the foundress's contribution, the y intercept). Male production by soldiers in O. tepperi 2 is consistent with no male soldiers being present in this population to act as a source of sperm. In population O. tepperi 1, where soldier males were present, there was no association between number of female soldiers with the number of male dispersers present in the gall (r2 =.03, p =.62). Therefore, we have no evidence for soldier production of males in this population.
Concordance of estimates from microsatellite data and data from
ovarian dissections and census
We analyzed concordance of the microsatellite data with the ovarian
dissection and census data via the correlations between the soldier
reproduction estimates from the two methods. Microsatellite per capita
estimates (of female production) were positively correlated with ovarian
dissection and census estimates (of male and female production; r
=.722), but this relationship was not significant (p =.168,
n = 5). However, there was a strong and significant correlation
between per capita dissection and census estimates, and the per capita
microsatellite estimates, when soldiers are assumed to produce all of the male
dispersers (r =.891, p =.0425, n = 5).
Inference of ancestral states of reproductive differentiation
To understand the evolution of soldier reproduction, we mapped census and
microsatellite estimates onto a phylogeny of Australian gall-inducing thrips
(Figure 1). The three
relatively basal species with soldiers (K. hamiltoni, O. morrisi, and
O. waterhousei) had substantially higher soldier reproduction than
the derived species O. tepperi and O. habrus. Character
optimization using squared-change parsimony in MacClade
(Maddison and Maddison, 1992)
shows that levels of inferred ancestral reproductive differentiation were
relatively low at more-basal nodes (Figure
1).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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This is the first evidence, from both genetic and phenotypic data, conclusively demonstrating soldier reproduction in thrips and putting soldier reproduction in an explicitly phylogenetic context. Analysis of ovarian dissection and census data, and microsatellite data, indicates that average levels of reproductive differentiation between foundresses and soldiers vary substantially between species. Reproductive differentiation is relatively low in K. hamiltoni, O. waterhousei, and O. morrisi, but there was substantially higher differentiation in O. tepperi and O. habrus. Indeed, microsatellite data analysis for two O. habrus and two O. tepperi populations indicate that some soldiers in these species may approach functional sterility.
In our study, estimates of soldier reproduction using chorionated oocyte counts and regression analysis are higher than estimates made using genetic data. One difference between methods is that genetic estimates are based on female disperser production only, whereas census estimates include production of both males and females. If soldiers produce more males than the foundress does, then genetic data will underestimate egg production by soldiers. We observe that where sex ratios are highly female biased (i.e., in K. hamiltoni and O. tepperi), per capita production by soldiers relative to foundress falls within or close to the range of microsatellite-based estimates. Moreover, per capita microsatellite-based estimates under the assumption that soldiers produce all of the male dispersers exhibit a higher correlation with per capita census estimates than do the microsatellite-based estimates without this assumption.
A second difference between methods is that census data estimates assume that all chorionated oocytes will result in viable offspring, while microsatellite estimates use only genotypes of adult thrips. If this assumption is violated, as a result of egg retention or egg resorption by soldiers, then census data provide overestimates of soldier reproduction. We conclude that the genetic estimates are more likely to be underestimates of the true level of soldier reproduction, and the census data are more likely to provide overestimates. However, these differences do not affect our conclusions that soldiers often produce a substantial proportion of dispersers within a colony and that reproductive differentiation differs markedly between species.
From our phylogenetic pattern of lower levels of reproductive
differentiation in more basal lineages
(Figure 1), we infer that
soldier morphology and behavior evolved in the context of substantial levels
of reproduction by soldiers and that reduced reproduction by thrips soldiers
has evolved more recently. Factors directing this change to reduced soldier
reproduction are unknown. However, we note that an association may exist
between the evolution of decreased gall size
(Crespi and Worobey, 1998) and
a decrease in soldier reproduction. Soldier reproduction in small galls may be
limited by space, and female soldiers may not be inclined to replace highly
related sisters with their own less related daughters
(Kranz et al., 1999;
Ratnieks, 1988).
Our evidence for thrips indicates that morphological differentiation
evolved before strong reproductive division of labor. Might similar patterns
exist for other taxa with soldiers? In aphids, willingness to defend a clone
apparently evolved first, followed by morphological specialization for
defense, with soldiers initially capable of molting to adulthood
(Stern and Foster, 1997). Time
spent as a soldier instar may have increased until there was selection for a
split in developmental pathways that allowed a more rapid development of
nonsoldiers. Ultimately, in some species, soldiers delayed molting until they
became obligately sterile. Termite soldiers may also have evolved under high
levels of reproduction in Archotermopsis, which are regarded as the
most socially primitive termites (Thorne,
1997), all soldiers have well-developed gonads, and similar
apparent high levels of soldier reproduction are known from other species in
the primitive family Termopsidae (Myles,
1986).
Thrips, termites, and aphids may thus share a similar scenario for the
origin of the helpers, which involved the emergence of helping behavior and
morphological specialization in association with the retention of substantial
reproduction, followed by a decrease in reproduction in some lineages. In
contrast, the evolution of helping in Hymenoptera involved the origin of
workers being directly and immediately associated with marked reproductive
division of labor, and both preceded morphological differentiation
(Bourke and Franks, 1995;
Wilson, 1971). We suggest that
acting as a soldier during rare, episodic colony invasions involves less of a
trade-off between helping and reproduction than does acting as a Hymenopteran
worker and engaging in the daily activities of foraging or brood care. The
energetic demands of worker tasks may direct energy away from reproduction,
while there are no increased energy demands on soldiers when a colony is not
threatened except in the case of gall cleaning, or patrolling the gall
surface, in some species of social aphids
(Benton and Foster, 1992;
Stern and Foster, 1996). We
also note that soldier morphology may make physical and reproductive
domination of helpers by foundresses more difficult than in taxa without such
morphological specializations for fighting. The differences between taxa with
soldiers and taxa with workers may ultimately derive from aspects of ecology,
as taxa with soldiers inhabit defensible factory fortresses, while in many
taxa with workers, helping behavior apparently evolved in the context of high
forager mortality and "life insurance" for the helpless brood
(Crespi, 1994;
Queller and Strassmann,
1998).
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ACKNOWLEDGEMENTS |
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We thank F. Breden, J.H. Law, C. Peeters, J. Strassmann, J. Taylor, and P.M. Willis for useful comments and discussion. This work was supported by the Natural Science and Engineering Council of Canada, the Australian Research Council and the U.S. National Geographic Society.
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