biology of a new species of socially parasitic thrips ... · foederatus paracholeothrips mulgae...

Biology of a new species of socially parasitic thrips(Thysanoptera: Phlaeothripidae) inside Dunatothripsnests, with evolutionary implications for inquilinismin thrips

JAMES D. J. GILBERT1,2*, LAURENCE A. MOUND3 and STEPHEN J. SIMPSON1

1A08 Heydon-Laurence Building, University of Sydney, NSW 2006, Australia2UNSW Arid Zone Research Station, School of Biological, Earth and Environmental Science,University of New South Wales, NSW 2052, Australia3CSIRO Ecosystem Sciences, GPO Box 1700, Canberra, ACT 2601, Australia

Received 11 January 2012; revised 24 March 2012; accepted for publication 25 March 2012bij_1928 1..11

Akainothrips francisi sp. nov. is shown to be an inquiline (i.e. it invades, and breeds within, domiciles of anotherspecies). Currently, its only known host is Dunatothrips aneurae, a subsocial thrips that creates silken domicilesby securing together phyllodes of mulga (Acacia aneura) in the arid zone of Australia. We found Ak. francisiprolifically breeding inside live D. aneurae host domiciles, both immature and mature. Akainothrips francisi did notkill its host and we saw no evidence of antagonistic host-inquiline interactions. This is thus the seconddemonstrably inquiline species of Acacia thrips, although other possible inquilines have been suggested includingtwo Akainothrips. We found that Ak. francisi occurred with positive density dependence, and was associated withmoderately reduced host reproduction. This latter association was especially evident in larger host domiciles,suggesting that Ak. francisi either inhibits further host reproduction after invasion or exploits poor quality hostsmore successfully. Sex ratios were slightly female biased. Akainothrips francisi males were exceptionally variablein size, colour, and foreleg size compared to females, with morphs co-occurring within domiciles, suggesting sexualselection and the possibility of different male reproductive strategies. The discovery of Ak. francisi highlightsparticular morphological affinities among known or suspected inquiline Acacia thrips within Akainothrips andother genera, allowing us to hypothesize a common origin of this lifestyle from within Akainothrips. © 2012 TheLinnean Society of London, Biological Journal of the Linnean Society, 2012, ••, ••–••.

ADDITIONAL KEYWORDS: commensalism – dealation – eusociality – Hymenoptera – social parasitism –subsociality.

INTRODUCTION

Virtually all known social insect groups have a dis-tinct suite of exploiters (Wilson, 1971), testifying tothe intrinsic value of the social nest as a breedingresource. These exploiters usually benefit from host-derived resources and, because their effect upon hostfitness is typically negative, they are often called‘social parasites’. Within these exploiter communitiesare many ‘inquilines’, which is a term derived fromthe Latin for ‘guest’ (Brown, 1956). Inquilines in euso-cial colonies are widespread and intensively studied

(Redford, 1984; Hölldobler & Wilson, 1990; Busch-inger, 2009), but inquilines also occur within nests ofnon-eusocial insects (e.g. aphids: Miller & Crespi,2003; psyllid bugs: Yang, Mitter & Miller, 2001; ceci-domyiid flies: Skuhravá, Skuhravy & Brewer, 1984;cynipid wasps: Roskam, 1992). In eusocial colonies,inquilines are defined as ‘permanent parasites that donot enslave their host and do not produce workers’(Buschinger, 2009: 222), but outside of the eusocialcontext, ‘inquiline’ is not strictly defined. Rather, it isused in a broad sense to denote a species that obli-gately lives and breeds within the nest of anotherspecies, being unable to produce its own nest (Miller,2004), although without actively destroying its host*Corresponding author. E-mail: [email protected]

Biological Journal of the Linnean Society, 2012, ••, ••–••. With 4 figures

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© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ••, ••–•• 1

(Forsyth & McCallum, 1978; Yang et al., 2001). Thisdistinguishes inquilines from kleptoparasites, whichactively usurp the host nest and kill or evict the host.Nevertheless the inquiline may negatively affect thehost through, for example, competition for resources(Morris, Mound & Schwarz, 2000) or space (Passera,Gilbert & Aron, 2001) and thus may correctly beunderstood as a social parasite.

In the arid zone of Australia, low humidity andintense sunlight create a very hostile, desiccatingenvironment in which an enclosed nest is a parti-cularly valuable resource, making it an especiallyattractive prospect for social parasites. One suchnest-building group is the Australian Acacia thrips(Thysanoptera: Phlaeothripinae). As haplodiploids,Acacia thrips are genetic analogues of the socialHymenoptera, and are rapidly becoming a parallelmodel system containing a microcosm of social evolu-tion (Crespi, Morris & Mound, 2004). Amongst manyothers, the Phlaeothripinae contains a clade of gall-inducing species, many of which have co-speciatedwith their Acacia host plants, probably during periodsof rapid diversification brought on by climate change(McLeish, Chapman & Schwarz, 2007), as demonstra-etd by parallel radiations of hosts and gall-inducers(Crespi et al., 2004; McLeish et al., 2007). Immediatelyrelated to this clade is a separate group of gall-targeting kleptoparasites that have mostly evolved ahigh degree of host specificity (Crespi & Mound, 1997).A further clade contains whole genera that build‘domiciles’ by securing phyllodes together with silk(Mound & Morris, 2001). Although less well-studied,recent research has documented an expanding suiteof thrips species associated with domicile-buildingAcacia thrips that rivals that of the gall thrips (Mound& Morris, 2000; Bono, 2007) (Table 1). Active domicilesare subjected to usurpation by multiple species ofkleptoparasites, often species-specific, and old, emptydomiciles are frequently occupied by opportunisticinvaders.

Although several Acacia thrips species are suspectedto be inquilines within domiciles (Mound & Morris,2000; Bono, 2007), surprisingly, only one has ever beenformally described as such (Advenathrips inquilinus;Morris et al., 2000). A few thrips species have beenrecorded cohabiting with hosts within domiciles(Mound & Morris, 2000), suggesting at least the pos-sibility of an inquiline lifestyle. However, given that allthrips are likely to show thigmotactic behaviour (i.e.seeking small spaces; Kirk, 1997), finding the occa-sional specimen, or even relatively large numbers,inside a domicile may mean nothing more than thatthe insects are seeking shelter. Most of these specieshave never been taken in sufficient numbers to inferany details about their relationships or interactions,beyond the mere fact of cohabitation. In a notable

exception, Bono (2007) recorded heterospecifics foundin Dunatothrips domiciles, as well as their effect uponsurvival of host foundress(es). Heterospecifics weremore frequent in pleometrotic species (i.e. where domi-ciles are often cofounded). Two species of Akainothrips,supposedly a genus of opportunistic inhabitors ofabandoned domiciles, were found living inside activedomiciles of Dunatothrips aneurae, presumably asinquilines (Bono, 2007). Those two species were foundto impose a moderate degree of mortality upon theirhost, and their occurrence was related to the density ofdomiciles on the host tree.

In the present study, we describe a new species ofinquiline thrips, Akainothrips francisi sp. nov.,that, unambiguously, invades and breeds withinactive domiciles of D. aneurae Mound (Phlaeothripi-nae) on Acacia aneura. We provide details of thecohabitation and reproduction of the new specieswithin host domiciles, and demonstrate a mildly butsignificantly deleterious association between the pres-ence of Ak. francisi and both host survival and repro-duction, even in the absence of any aggressiveinteractions between the two species. These observa-tions indicate its inquiline habit and suggest compe-tition for resources and/or space within a domicile. Wealso repeat for the new species an analysis conductedby Bono (2007) by showing that its distribution isdependent upon host domicile density. Based upon itstaxonomic affinities, we provide a tentative hypoth-esis for a single common origin of the inquiline lif-estyle among the Australian Phlaeothripinae.

MATERIAL AND METHODS

Acacia thrips fall into two monophyletic groups ofwhich one contains all domicile-constructing thrips(Dunatothrips, Paracholeothrips, Carcinothrips, Sar-trithrips, and Panoplothrips; Morris et al., 2002).Dunatothrips aneurae lives entirely within domicilesformed from the phyllodes of Ac. aneura, which thethrips tie together using silk extruded from abdomi-nal segment 10 (the tube characteristic of all Tubu-liferan thrips). Domiciles are frequently cofounded(Morris et al., 1999) by up to 21 foundress femalesand at least one male (J. D. J. Gilbert, pers. observ.).Foundresses become dealate upon nesting and remainwithin the domicile their whole lives. During thistime, they produce a brood of offspring that matureswithin the domicile, with most dispersing, whereas afew remain and become dealate within (or in anextension of ) the natal domicile. In the field, domi-ciles are found containing the original foundressesplus offspring at all stages of development. ActiveD. aneurae domiciles are commonly attacked by thekleptoparasite Xaniothrips mulga Mound (Bono &Crespi, 2006), possibly the inquiline Ad. inquilinus

2 J. D. J. GILBERT ET AL.

© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ••, ••–••

Tab

le1.

Spe

cies

asso

ciat

edw

ith

dom

icil

e-bu

ildi

ng

thri

pson

Aca

cia

Gen

us

Spe

cies

Hos

tth

rips

Hos

tpl

ant

Ass

ocia

tion

Ref

eren

ce

Aka

inot

hri

psfr

anci

siD

un

atot

hri

psan

eura

eA

caci

aan

eura

Inqu

ilin

eP

rese

nt

stu

dyA

kain

oth

rips

grem

ius

Du

nat

oth

rips

aneu

rae,

Du

nat

oth

rips

gloi

us

Aca

cia

aneu

ra,

Aca

cia

lysi

phlo

iaL

ikel

yin

quil

ine

(coh

abit

sw

ith

hos

t;as

soci

ated

wit

hin

crea

sed

hos

tm

orta

lity

)

Bon

o(2

007)

[Du

nat

oth

rips

aneu

rae]

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resp

iet

al.

(200

4)[D

un

atot

hri

psgl

oiu

s]A

kain

oth

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sp.

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nat

oth

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aneu

rae

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cia

aneu

raL

ikel

yin

quil

ine

(coh

abit

sw

ith

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t;as

soci

ated

wit

hin

crea

sed

hos

tm

orta

lity

)

Bon

o(2

007)

Ad

ven

ath

rips

inqu

ilin

us

Du

nat

oth

rips

vest

itor

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Du

nat

oth

rips

aneu

rae

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cia

aneu

raIn

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ris

etal

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Sch

war

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glyp

his

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sken

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ten

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ta(Q

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but

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th

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nd

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s(2

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(200

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(200

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Kle

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Aca

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(199

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(200

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.(2

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.(2

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a,si

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ns,

teph

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al.

(200

4)

A NEW INQUILINE THRIPS 3


(Morris et al., 2000), and two species of Akainothrips,probably inquilines (Bono, 2007).

No molecular evidence is available for Akaino-thrips, and its phylogenetic placement is uncertain(Crespi et al., 2004). Akainothrips is one of the mostspeciose and morphologically variable genera ofAcacia thrips with 34 described species including Ak.francisi. Before the present study, all known Akaino-thrips were originally described as opportunists on avery wide range of Acacia species, occupying aban-doned domiciles, old galls, and crevices in wood,although with an apparently high level of host speci-ficity (whether this specificity refers to host-plant orhost-thrips is uncertain; Crespi et al., 2004). However,Ak. gremius and an undescribed Akainothrips haverecently been found within live D. aneurae domicilesand were thus referred to as inquilines (Bono, 2007).

The new species was found breeding in considerablenumbers within D. aneurae domiciles on Ac. aneura inSandstone and Bald Hills Paddocks, UNSW Arid ZoneResearch Station, Fowlers Gap, NSW, Australia(‘Fowlers Gap’), approximately 110 km north of BrokenHill (11 trees around 30°57.6′S, 141°42.4′E). Onehundred and forty-two domiciles of D. aneurae fromAc. aneura at sites around Fowlers Gap were collectedbetween October 2011 and March 2012. The number ofdomiciles present on each inhabited branch was noted.Domiciles were initially carefully dissected aiming notto disturb the live inhabitants; interactions betweenlive hosts and inquilines inside the domicile wereobserved for a few minutes under a binocular micro-scope. After dissection, adult thrips and eggs insideeach domicile were counted and identified. Nymphs ofeach stage of D. aneurae were counted. Nymphalstages of Ak. francisi present within each domicilewere noted, although their large numbers and mobilitytypically precluded counting. The volume of each domi-cile was assumed to be a cuboid, measured as thelength (longest dimension of silk) ¥ width (longestdimension perpendicular to length) ¥ depth (longestdimension perpendicular to width).

RESULTS AND DISCUSSION

We first describe the new species and its relationships;second, we give details of behaviour and biology.Finally, based on the inferred phylogenetic placementof the new species, we offer a tentative hypothesisabout the origin of inquilinism in thrips, and wediscuss the potential implications of this finding for ourunderstanding of the evolution of inquilinism.

AKAINOTHRIPS FRANCISI SP. NOV.Female macropteraBody, legs, and antennae mainly brown; fore tarsi andapical third of fore tibiae yellow, also hind tarsi and

extreme apex of hind tibiae; antennal segment IIIyellow in basal half, also IV at base; major setae pale,anal setae long and dark; forewing pale.

Head longer than wide (Fig. 1), cheeks convexwith one pair of stout setae on posterior third; eyesscarcely longer dorsally than ventrally; postocularsetae not distinguished from minor setae; maxillarystylets retracted to posterior margin of eyes, scarcelyone-fifth of head width apart medially; maxillaryguides well-developed, maxillary bridge weakly devel-oped. Antennae eight-segmented, III with one senso-rium, IV with three sensoria, VIII broad at base.

Pronotum transverse, weakly sculptured, notopleu-ral sutures complete; major setae – epimerals andposteroangulars long and weakly capitate, anteroan-gulars shorter and blunt, midlaterals and anteromar-ginals not distinguished from discal setae (Figs 4and 5). Metanotum weakly reticulate, anteromediallywith one to four (rarely 0) minor setae (Fig. 8),median major setae small and acute. Prosternal bas-antra usually not developed, sometimes one or bothsclerites weakly developed but small (Fig. 9); fernalarge, mesopraesternum represented by pair of lateraltriangles; sternopleural sutures long. Fore tarsuswith small, weakly curved tooth on inner margin nearapex. Forewing parallel-sided, sub-basal setae small;approximately six duplicated setae present.

Abdomen with pelta weakly recessed into anteriormargin of tergite II, reticulate, campaniform sensillapresent; III–VII with two pairs of sigmoid setae, bothpairs of posteroangular setae with apices blunt butweakly capitate on posterior tergites (Fig. 6); tergiteIX setae S1 and S2 weakly capitate; tube slender,anal setae long.

Measurements (holotype female in microns, small-est and largest females in parentheses). Body length2100 (1750, 2350). Head, length 230 (210, 250);median width 190 (170, 200). Pronotum, length 180(150, 210); width 260 (230, 310). Forewing length 850(720, 900); sub-basal setae 20. Tergite VI lateral setae35. Tergite IX setae, S1 75; S2 100. Tube length 160(150, 185); basal width 80 (70, 85); anal setae 250.Antennal segments III–VIII length 55, 50, 48, 45,40, 25.

Male macropteraVariable in size and colour; small males (Fig. 2) essen-tially similar to females, although the largest maleswith posterior two-thirds of head yellow (Fig. 3), alsothorax, forelegs, and abdominal segments I–VII.Small males with forelegs and pronotum similar tofemales. Larger males with pronotum wider, forefemora expanded, fore tibia toothed at inner apicalmargin, fore tarsus with long tooth. Abdominal tergiteIX setae S1 and S2 similar to female; sterniteswithout pore plates.



Measurements (smallest and largest paratypemales, in microns). Body length 1700, 2180. Head,length 220, 240; median width 170, 190. Pronotum,length 160, 260; width 230, 350. Forewing length 650,850. Tergite IX setae, S1 65, 75; S2 75, 65. Tubelength 135, 160.

ETYMOLOGY

The species is named for Dr Francis S. Gilbertin recognition of his invaluable and continuing con-tributions to the fields of evolutionary ecology andentomology.

TYPE SERIES

Female holotype, Australia, New South Wales,Fowlers Gap, 110 km N of Broken Hill, from domicileof Dunatothrips aneurae on Acacia aneura, 15.xi.2011(Gilbert JDJ), in Australian National Insect Collec-tion, CSIRO, Canberra.

Paratypes, 14 females, eight males, from samedomicile as holotype; 14 females, nine males fromother domiciles at same locality and date.

Nonparatypes: South Australia. Port Augusta,four females, three males from Acacia aneura, iii.2005(J. Bono); one male ‘South Australia. Jeremy Bono’,

with no further details; New South Wales. 10 kmwest of Mutawingi, one male (J. Bono) with no host ordate; 92 km south west of White Cliffs, two females(J. Bono) with no host or date. Northern Territory.105 km north of Alice Springs, one female fromAcacia aneura phyllode glues, 3.iii.1996 (D. Morris).

RELATIONSHIPS

This new species can be identified as a species ofAkainothrips using the generic key provided in Crespiet al. (2004). It shares the suite of character statesgiven in the diagnosis for that genus, differing only inhaving the maxillary bridge within the head moreweakly developed and the ventral surface of the eyesmore extensively developed. It shares with 14 of the33 previously described species of Akainothrips thecharacter state of several minor setae being presenton the anterior half of the metanotum (Fig. 8),although the number of such setae is variable, and ina few specimens they are not present. Among these 14species, only nyngani shares the following three char-acter states: body of female uniformly brown; fourthantennal segment with three sensoria; female foretarsus with a lateral tooth. From nyngani, this newspecies differs in having the maxillary stylets much

Figures 1–3. Akainothrips francisi sp. nov. (1) Female holotype; (2) Small male; (3) Large male.



closer together in the head, the antennal segmentsmore extensively brown, the pronotal posteroangularsetae well developed, and the tergal lateral setae notbroadly capitate. Considering the 19 species that lackmetanotal minor setae (this condition being shared bya few individuals of francisi), only a few share thethree character states indicated above for nyngani,together with the absence of major postocular setae.Among species with this suite of characters, the mostclosely similar is carniei, although that has the majorsetae with much more broadly expanded apices thatare strongly asymmetric on the tergites, and the hindtibiae are yellow on the distal third. The few speci-mens from which carniei is known also came fromBroken Hill, although they were taken from Acaciacarneorum. One further species, Akainothripsgremius, has been reported from Acacia aneura(Crespi et al., 2004; Bono, 2007), although there arefew voucher specimens available to support thesereports apart from four paratypes taken near Alice

Springs. This species shares with Ak. francisi thepresence of additional metanotal minor setae, and isvery similar in general body form and colour.However, the females of Ak. gremius lack a fore tarsaltooth, and both pairs of lateral setae on the medianabdominal tergites are capitate and approximately100 microns in length, which is approximately as longas the length of a tergite. Amongst the small brownspecies of this genus, only Ak. francisi has the lateralsetae short and blunt on tergites IV–VI, scarcely 35microns in length and approximately half as long asa tergite (Fig. 6).

BIOLOGY

Out of 153 active D. aneurae domiciles collected, 41(26.7%) contained Ak. francisi. Where present, 1–23adult Ak. francisi were found living within each domi-cile. Adult D. aneurae within domiciles numberedbetween 0 and 81. In nine cases, live D. aneurae

Figures 4–9. Akainothrips francisi sp. nov. (4) Pronotum small male; (5) Pronotum large male; (6) Abdominal tergitesV–VI; (7) Antennal segments II–VII; (8) Metanotum; (9) Thoracic sternites.



offspring were found in a domicile without anydealate foundresses present; these were excludedfrom analyses involving foundress numbers. In addi-tion, three domiciles disintegrated before volumecould be measured; these were excluded from analy-ses involving domicile volume.

Several lines of evidence indicate that Ak. francisiis an inquiline in the broad sense defined above. First,most infested host domiciles (37 out of 41 domiciles;90.2%) contained at least one live Ak. francisi, butin only five out of 41 infested domiciles (12.2%) wereall the host D. aneurae dead, indicating that Ak.francisi does not actively kill its host. Nevertheless,supporting Bono (2007), the proportion of hostfoundresses alive upon dissection was negativelyassociated with numbers of Ak. francisi adultspresent [binomial general linear model (GLM), likeli-hood ratio test (LRT): c2 = 24.0, d.f. = 1, P < 0.001,N = 144; Fig 10A].

Second, Ak. francisi was clearly breeding withinhost domiciles: of 41 domiciles that contained Ak.francisi, eggs of the intruder were present in 26(63.4%) and numbered from 1 to > 500 (median ± SD,59.1 ± 111.4). Eggs of D. aneurae and Ak. francisiwere readily distinguished under a microscope bysize, colour, and texture (Fig. 11). Nymphs of Ak.francisi were present in 22 infested domiciles (53.7%)alongside offspring of D. aneurae, frequently outnum-bered host offspring, and occurred at all stages ofdevelopment from egg to adult, indicating that Ak.francisi relies upon host domiciles throughout its lifecycle. Moreover, Ak. francisi were commonly found indomiciles with only immature D. aneurae offspring(11 out of 41 domiciles; 26.8%), in contrast to Ad.inquilinus, which was only found in mature Dunato-thrips domiciles (Morris et al., 2000). Although foundthree times in old abandoned Dunatothrips domiciles,Ak. francisi were never found alone inside a healthydomicile despite extensive searching, suggesting thatthey are unable to produce or maintain a domicile oftheir own.

Third, no antagonistic inquiline/host interactionsand no directly adverse effects of the inquiline wereobserved; indeed, no behavioural interactions wereobserved between host and inquiline at all, eventhough the two species were regularly observed inphysical contact. The absence of inquiline/host inter-action has been observed before (Miller, 2004; Rosa,Marins & DeSouza, 2008). Bono (2007) suggestedthe possibility of lethal fighting between host andinquiline thrips; based on our findings, we regard thisas unlikely, although we cannot rule out aggressionupon invasion by the inquiline. Rather, this findingsuggests manipulation by the inquiline; for example,(1) chemical camouflage/mimicry of hosts byinquilines, similar to some inquilines of ant and

termite nests (Howard, McDaniel & Blomquist, 1982;Lenoir, Malosse & Yamaoka, 1997; Akino et al., 1999)or (2) exploitation of the host’s tendency to cofounddomiciles, which requires suppression of aggressiontowards conspecifics and may have involved completesuppression of aggression towards all invaders (Höll-dobler & Wilson, 1990; Ronquist, 1994; Miller, 2004;Bono, 2007). Dunatothrips aneurae offspring alsooccasionally breed within or adjacent to natal domi-ciles (Bono & Crespi, 2006), expanding them to incor-porate additional phyllodes; this phenomenon mayalso promote inquiline invasion, although its preva-lence and importance requires further research.Although not mutually exclusive, a ‘mimicry’ hypoth-esis would predict a degree of host specificity forinquilines (as occurs in butterfly inquilines of antnests; Akino et al., 1999), whereas a ‘tolerance-exploitation’ hypothesis would predict that, because ofhost tolerance, inquilines could theoretically targetany of several pleometrotic Dunatothrips species(Crespi et al., 2004); further data would allow a test ofthese hypotheses.

DENSITY DEPENDENCE

The proportion of domiciles infested by Ak. francisiwas strongly related to the number of domiciles ona branch (binomial GLM, LRT, N = 31 branches,c2 = 10.8, d.f. = 1, P < 0.001; Fig. 10B). This supportsthe pattern found by Bono (2007) for Akainothrips sp.and Ak. gremius, and, as in that case, is probablyrelated to limited dispersal in D. aneurae, resulting inlocally dense aggregations (Bono & Crespi, 2006,2008; J. D. J. Gilbert and S. J. Simpson, unpubl.data). Such aggregations may be more conspicuous toprospecting Ak. francisi, and, once infested, mayreduce the need for dispersal in subsequent genera-tions of the inquiline. In addition, this local crowdingmay facilitate pleometrosis in Dunatothrips (J. D. J.Gilbert and S. J. Simpson, unpubl. data, but see alsoBono & Crespi, 2006), which in turn may facilitateinvasions by exploiters (Ronquist, 1994; Miller &Crespi, 2003).

NEGATIVE ASSOCIATION WITH HOST REPRODUCTION

We found evidence that the inquiline was associatednegatively with host reproduction, suggesting compe-tition for space or resources, or that inquilines arebetter at exploiting poor-quality hosts. First, eventhough adults of the two species showed no antago-nistic interactions, the number of Ak. francisi eggs ininfested domiciles was negatively associated with thetotal number of D. aneurae offspring (Poisson GLM,LRT, N = 41: c2 = 24.2, d.f. = 1, P < 0.001; Fig. 10C)and marginally so with per-foundress offspring (linear



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Figure 10. A, proportion of Dunatothrips aneurae hosts found alive in nests containing different numbers of the inquilineAkainothrips francisi. Bars show estimates (±SE) from the binomial model. Raw data are shown for clarity. B, proportionof domiciles infested by Ak. francisi according to the number of domiciles present on a branch. Number of D. aneurae hostoffspring per domicile (C) and per foundress (D) associated with different numbers of Ak. francisi eggs. Number ofD. aneurae host offspring per domicile (E) and per foundress (F) in small (< 284 mm3) and large domiciles (> 284 mm3) inthe presence and absence of Ak. francisi. B, C, D, E, F, boxes show medians ± interquartile range; whiskers show 95%confidence intervals, with outliers plotted separately.



model, square-root transformed, N = 38: F1,37 = 3.26,d.f. = 1, P = 0.08; Fig. 10D). This does not by itself ruleout, for example, oophagy by the inquiline. Second,however, the inquiline was associated with the great-est decline in host reproduction in larger-volumedomiciles. In domiciles smaller than the mean volume(284 mm3), inquiline presence was not associated withhost reproduction, whereas, in larger domiciles, totalhost reproduction was strongly reduced in the pres-ence of the inquiline compared to similarly-sized,uninfested domiciles (Poisson GLM, LRT, c2 = 24.4,d.f. = 1, P < 0.001, N = 150; Fig. 10E). Per-foundressreproduction showed a similar pattern (linear model,square-root transformed, N = 141; F1,137 = 6.38,P = 0.01; Fig. 10F). One possibility is that, ratherthan directly destroying brood, the inquiline inhibitsany further reproduction by the host that would bepossible in a larger domicile. This may be achieved bya faster reproductive rate than the host (inquilineeggs are smaller and usually more numerous). Inter-estingly, faster reproductive rates than hosts werealso suggested for Vicinothrips bullatus (Bono, 2007).As an alternative explanation, reduced host reproduc-tion may be a cause rather than a consequence ofsuccessful inquiline reproduction: inquilines may beable to exploit the space in a large domicile that is leftby host foundresses of low fitness that fail to repro-duce sufficiently quickly to fill it. Competitive effectsof inquilines upon host fitness are poorly studied.Inquiline Plagiolepis ant queens are known to becapable of displacing host queens within their ownnests (Passera et al., 2001), and Leptothorax acer-vorum queens infested with Leptothorax pacisinquilines suffer mildly reduced fertility withoutphysical damage, although the mechanism isunknown (Buschinger, 1990). Similarly, Tamalia

aphids suffer reduced fertility when infested withinquiline congeners, despite the lack of any obviousantagonistic interactions (Miller, 2004).

BODY SIZE VARIATION, SEX, AND MORPH RATIOS

We found no evidence that the inquiline habit has ledto miniaturization of adults, as has been found ininquiline members of some other orders, notably ants(Bourke & Franks, 1991; Buschinger, 2009). Akaino-thrips francisi is not a particularly small exemplar ofits genus (by contrast, pronotum widths for mostknown Akainothrips spp are listed by Crespi et al.,2004: mean 238 microns, range 185–350 microns);adult Ak. francisi are only slightly smaller than hosts(D. aneurae pronotum width 335 microns; Crespiet al., 2004), as are the two likely inquiline Akaino-thrips studied by Bono (2007), which are approxi-mately 90% of host size (J. Bono, pers. comm.).

Crespi et al. (2004) point out that males of knownAkainothrips species are often unusually variable insize, suggesting sexual selection. Consistent withthis, adult Ak. francisi are variable in size, particu-larly males. Moreover, larger males (pronotum width> 300 microns) have the body and forelegs yellow incolour, whereas medium and small males (pronotumwidth < 290 microns) are as brown as females.Females also vary in body size but without colourvariation. There is no evidence that size variation ineither sex is other than continuous. The forelegs oflarger males have the femora considerably expanded,the tibial tooth larger, and the fore tarsal tooth muchlarger. A male with the pronotum 230 microns widehas the forelegs indistinguishable from those offemales (Fig. 2), but males with the pronotum from300 to 350 microns wide (Fig. 3) have foreleg arma-ture that has been shown in other species to beassociated with fighting (Crespi, 1992).

We counted sex and male morph ratios in 30domiciles, and measured males from eight domiciles.The adult sex ratio was marginally female-biased(median ± SD 0.66 ± 0.39, c2 = 38.9, d.f. = 27, P = 0.06;female range 0–15, male range 0–8), as is that ofthe host species (Bono & Crespi, 2008), suggestinglocal mate competition among males (Frank, 1987).Of domiciles where males were measured, four con-tained multiple males. In all four domiciles, malesshowed striking size variability within a domicile. Inone domicile containing eight males, pronotal widths(microns) were: 250, 260, 275, 275, 280, 300, 320, 350;the largest two males were yellow, whereas theremaining males were brown. Brown males appearedsingly four times but, otherwise, were always accom-panied by one or more yellow males; in contrast, up tothree yellow males were found sharing a domicilewithout brown males. The ratio of large yellow males

Figure 11. Eggs of Dunatothrips aneurae (Da, hatched)beside those of the inquiline Akainothrips francisi (Af,unhatched).



to small brown males was not different from 1 : 1(0.50 ± 0.41, yellow male range 0–3, brown malerange 0–6). Male interactions have yet to be observedin this species. However, the potential appears toexist for sexual selection operating on Ak. francisimales with the clear possibility of multiple malereproductive strategies.

ORIGIN OF INQUILINISM IN ACACIA THRIPS

Akainothrips francisi is only the second species ofdemonstrably inquiline Acacia thrips to be described,the first being Ad. inquilinus (Morris et al., 2000). Ofthese two, Ak. francisi is perhaps more clearly aninquiline because it was found living and breedingeven in immature domiciles of its host, whereas Ad.inquilinus was only ever found in mature host domi-ciles (Morris et al., 2000). Akainothrips francisiclearly does not actively kill its hosts, althoughwe have identified a negative association betweeninquiline and host reproduction. More data arerequired (for both Ak. francisi and Ad. inquilinus) totest whether or not this inquiline habit is genuinely(1) obligate or (2) host-specific.

Although Akainothrips are mostly opportunisticinhabitors of old domiciles of various insect taxa, inthe present study, we have shown that at least oneAkainothrips is an inquiline; at least two more arelikely to share this trait (Bono, 2007). Morphologicalaffinities among Akainothrips and those thripsspecies known or suspected to be inquilines inAcacia domiciles suggest a single origin of this lif-estyle, and one that is relatively recent. BesidesAkainothrips, among other ‘exploiter-type’ generaof thrips targeting phyllode-glued domiciles, threehave been observed cohabiting with hosts and havebeen assumed to be inquilines (Schwarzithrips +Advenathrips + Crespithrips) (Table 1). Based ontheir morphology, these three species have previ-ously been hypothesized to fall into one clade (Crespiet al., 2004); together with Vicinothrips, they sharemany structural character states with Akainothrips(Crespi et al., 2004). Taken together, these observa-tions suggest the hypothesis that the inquiline habitarose within Akainothrips and gave rise to a clade ofinquilines targeting various species of Dunatothrips.If true, this scenario would imply that theseinquiline thrips species, unlike many eusocialinquilines, do not follow ‘Emery’s rule’ (Le Masne,1956; Hölldobler & Wilson, 1990; Bourke & Franks,1991; Buschinger, 2009), in that they did not eachdiverge directly from their respective hosts. Rather,this would suggest they diversified onto differentDunatothrips hosts subsequently to a common originof the inquiline lifestyle. The available moleculardata (Crespi et al., 2004: 32) placed Vicinothrips and

Advenathrips within a discrete clade of ‘exploiters’,although no data were available at that time for anyAkainothrips species; further molecular data wouldfacilitate a phylogenetic analysis of this group and atest of Emery’s rule in Acacia thrips.

ACKNOWLEDGEMENTS

This work was paid for by an ARC Laureate Fellow-ship to SJS. The authors would like to thank K.Leggett and G. and V. Dowling for invaluable assis-tance with logistics, B. Crespi and J. Bono for helpfuldiscussions and for providing GPS locations anddirections to several host trees, M. Schwarz and S.Bonser for useful conversations, and two anonymousreferees for their comments. The authors declare noconflicts of interest, financial or otherwise.

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