Colony-specific Hydrocarbons Identify Nest Mates in Two Species of Formica Ant

Abstract

The possession of a colony identity is a fundamental property that underlies much animal behavior. In insect societies, it is widely accepted that nest-mate recognition cues are encoded within the cuticular hydrocarbons. Despite numerous studies over the past 30years, the identification of these nest-mate specific signatures is only just starting to occur. In this paper, we show two different methods by which nest-mate-specific signatures can be encoded within the hydrocarbon profile of two species of Formica ants. In F. exsecta, nest-mate-specific signatures rely on the distribution of chain lengths of a single type of hydrocarbon, various (Z)-9-alkenes, which are present in colony-specific proportions. In F. fusca, variation in nine different positional isomers of C25-dimethylalkanes is sufficient to produce unique colony profiles. By using this information alone, we correctly assigned 97 F. exsecta workers into their respective 20 colonies and 111 F. fusca workers into their respective 30 colonies. These two systems or variations of them may be expected to occur in many insect societies that have a strong colony identity. (PUBLICATION ABSTRACT)

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J Chem Ecol (2008) 34:10721080 DOI 10.1007/s10886-008-9482-7

Colony-specific Hydrocarbons Identify Nest Mates in Two Species of Formica Ant

Stephen J. Martin & Heikki Helanter &

Falko P. Drijfhout

Received: 9 January 2008 /Revised: 27 March 2008 /Accepted: 23 April 2008 /Published online: 18 June 2008 # Springer Science + Business Media, LLC 2008

Abstract The possession of a colony identity is a fundamental property that underlies much animal behavior. In insect societies, it is widely accepted that nest-mate recognition cues are encoded within the cuticular hydro-carbons. Despite numerous studies over the past 30years, the identification of these nest-mate specific signatures is only just starting to occur. In this paper, we show two different methods by which nest-mate-specific signatures can be encoded within the hydrocarbon profile of two species of Formica ants. In F. exsecta, nest-mate-specific signatures rely on the distribution of chain lengths of a single type of hydrocarbon, various (Z)-9-alkenes, which are present in colony-specific proportions. In F. fusca, variation in nine different positional isomers of C25

dimethylalkanes is sufficient to produce unique colony profiles. By using this information alone, we correctly assigned 97 F. exsecta workers into their respective 20 colonies and 111 F. fusca workers into their respective 30 colonies. These two systems or variations of them may be expected to occur in many insect societies that have a strong colony identity.

Keywords Formica . Cuticular hydrocarbons .

Nest-mate recognition . Alkenes . Dimethylalkanes

Introduction

The possession of a colony identity is a widespread feature among social insects. The ability to discriminate nest mates from non-nest mates is a fundamental property that underlies key behaviors, such as aggression, mate selection, and altruism. Despite its importance, the actual compounds that allow insects to discriminate between nest mates and non-nest mates remain elusive in all but a couple of ant species. The idea that cuticular chemistry plays a role in recognition in ants was suggested over 100 years ago (Fielde 1901, 1903) and has been the subject of much debate and research. It is now widely accepted that many social insects encode recognition cues in their cuticular hydrocarbon (CHC) profiles (Jackson and Morgan 1993; Howard and Blomquist 2005), which, in the Formica ants, are under a strong genetic influence (Beye et al. 1998, 2004). Although, initially, the evidence linking CHCs to nest-mate recognition was circumstantial (Breed 1998), direct experimental evidence obtained in recent years has demonstrated their involvement (Lahav et al. 1999; Akino et al. 2004; Ozaki et al. 2005; Martin et al. 2008a). However, despite over 30 years of research into the CHC profiles of a variety of insect societies, no compound or part of the profile has been identified that enables consistent discrimination of nest mate from conspecific non-nest mate over a large number of colonies. A key problem is that many other recognition signals, such as species, fertility, and task, also appear to be encoded within the same CHC profile as the colony-level, nest-mate signals (Denis et al. 2007), thus making identification of the individual signal components difficult. Furthermore, temporal and environmentally induced variations in CHC profiles may mask the more stable nest-mate recognition cues. As the signal strength of the various genetic and environmental cues varies with respect

S. J. Martin (*) : H. HelanterLaboratory of Apiculture and Social Insects, Department of Animal and Plant Sciences, University of Sheffield,Sheffield S10 2TN, UKe-mail: [email protected]

F. P. DrijfhoutChemical Ecology Group,School of Physical and Geographical Sciences, LennardJones Laboratory, Keele University, Keele ST5 5BG, UK

J Chem Ecol (2008) 34:10721080 10731073

Table 1 The mean correlation values (r2) between the relative amounts of major alkanes and alkenes in the cuticular hydrocarbon profile of Formica exsecta at species and colony levels

F. exsecta

Species, N=97 (20) Colonya, N=45 (20)

C23 vs. C25 0.46 0.730.24 C25 vs. C27 0.81 0.880.18 C27 vs. C29 0.58 0.860.17 C23:1 vs. C25:1 0.71 0.970.04

C25:1 vs. C27:1 0.47 0.980.04

C27:1 vs. C29:1 0.71 0.950.07

a The number of individuals analyzed (N) and number of colonies sampled (in parentheses) are given; error is represented by SD.

to the precise context, differences in the overall CHC profiles among individuals, castes, or colonies inevitably occur. Although the underlying causes of these differences are not known, researchers have attempted to discriminate signals by using sensitive multivariate statistical methods (principal component and discriminate analysis). These methods provide limited insight into what biological processes underlie the often very small differences detected, as they combine rather than separate out the various signals (Howard and Blomquist 2005). It is normally assumed that each peak or compound in a profile is an independent variable potentially containing information. However, what has long been known (Lockey 1988) but often overlooked is that the vast majority of CHCs (alkanes, alkenes, and monomethylalkanes) within any profile are structurally related, belonging to a homologous series in which the chain length increases by two carbons (e.g., C25, C27, and

C29), but the position of double bonds or methyl groups remains constant (e.g., 3-MeC25, 3-MeC27, and 3-MeC29).

In some insects, CHCs are produced with only one chain length or in highly limited homologous series; often, such CHCs are dominated by dimethylalkanes. Odd chain-length homologous series dominate the CHCs of most insects (Lockey 1988), and even-chain compounds, if present, are always in smaller proportions. However, if the ratios (relative amounts) of the compounds within a homologous series are constant [i.e., highly correlated (r2>0.9)] within a colony, population, or species, then that series can be treated as a single variable, greatly reducing the apparent complexity of the profile for multivariate analysis.

In order to decode the information contained within the CHC profile, we first investigated the CHC profiles of 13 species of Formica ants from geographically and ecologically different populations (Martin et al. 2008b). This allowed us to distinguish between species-specific cues, that must be common to all members of that species, and any potential colony-specific cues, that must vary between colonies but be consistent among colony members (nest

mates). This work revealed two species, F. fusca andF. exsecta, that had characteristics in their CHC profiles and behavioral traits that made them particularly suitable for further study. These characteristics were that (1) both species possess a strong colony identity as demonstrated by inter-colonial aggression (Wallis 1962; Czechowski 1990); (2) F. fusca has the most diverse CHC profile, with respect to dimethylalkanes, of any known Formica species (Martin et al. 2008b), and profiles of these compounds appeared to vary between colonies; and (3) F. exsecta has a simple CHC profile but retains a strong colony identity.

By studying the relationships of compounds within each homologous series and how these series form the CHC profile, from a large number of F. fusca and F. exsecta colonies, we provide evidence that only part of the CHC profile contains colony-specific information. Furthermore, this information is encoded in two quite different ways despite the two species belonging to the same genus.

Methods and Materials

Ant Samples

Groups of up to ten adult workers were randomly sampled from 30 F. fusca and 20 F. exsecta colonies at different

100

Relative percentage of dimethylalkanes, alkenes and alkanes

a b

C 21:1

C 21

C 23

C 23:1

C 25:1

C 25

C 27

C 27:1

C 29:1

C 29

C 31:1

C 31

C 23

C 25

C 27

3,7 dimeC 24

2,12 dimeC 24

11,15 diMeC 25

9,13 diMeC 25

7,11 diMeC 25

5,13 diMeC 25

7,15 diMeC 25

5,15 diMeC 25

5,17 diMeC 25

3,13 diMeC 25

2,12 dimeC 26

6,12 dimeC 26

8,12 dimeC 26

3,11 diMeC 25

Fig. 1 Variation in relative percentages of the major compounds (alkanes, alkenes, and dimethylalkanes) found in Formica exsecta (a) and F. fusca (b) at the species level. The variation for each compound was calculated within each chemical group; e.g., when only the alkanes were considered, C25 represents 6075% of the alkanes in F.

fusca. The compounds selected for further statistical analysis are shown in bold

1074 J Chem Ecol (2008) 34:10721080

locations in Finland during 2005 and 2006. All ants were sampled from ten locations within 30km of the Tvrminne Zoological Station in Hanko, south-western Finland. At all collection sites, both species occurred sympatrically in forest clearings created by logging. In total, 111 F. fusca and 97 F. exsecta workers were sampled. Ants were killed by freezing and stored individually in glass vials at 5C until extraction. F. exsecta colonies in this region are monogynous (Sundstrm et al. 1996), and only F. fusca colonies in which a single queen was found were used in this study, although workers may have been produced by more than one queen (Sundstrm et al. 2005).

Chemical Analysis

Individual ants were placed in glass vials, 50 l of high-performance liquid chromatography-grade hexane were added and extracted for 10 min. After this, ants were removed, the hexane allowed to evaporate, and the vials

sealed and stored at 5C. Just before analysis, 30 l of hexane were added to the vials. Samples were analyzed on an HP 6890 gas chromatograph (GC) connected to an HP5973 MSD (quadrupole) mass spectrometer (MS; 70 eV, electron impact ionization). The GC was equipped with an HP-5MS column (length, 30 m; ID, 0.25 mm; film thickness, 0.25 m), and the oven temperature was programmed from 70C to 200C at 40C min1 and then from 200C to 320C at 25C min1. Samples were injected in splitless mode, with helium as carrier gas, at a constant flow rate of 1.0 ml min1. CHCs were characterized by using standard MS databases, diagnostic ions, and Kovats indices. In F. exsecta, the double-bond positions of the alkenes were determined by dimethyl disulfide (DMDS) derivatization (Carlson et al. 1989) of four pooled extracts of ten adults that contained two ants from each colony chosen at random from the 20 colonies. In the few cases in which isomers of methyl-branched hydrocarbons overlapped, a characteristic ion of a compound was used to

Table 2 The average percentages (of the entire cuticular hydrocarbon profile) of six (Z)-9-alkenes in 20 Formica exsecta colonies, based on n1 samples

Colony code G H B J D I C F A E 8 60 22 56 71 35 64 40 53 69

N 5 5 5 10 4 5 4 5 10 5 3 4 4 4 4 4 4 4 4 4

C21:1 5 2 3 1

C23:1 36 29 24 22 12 12 4 6 4 4 34 32 26 20 6 7 6 6 5 4

C25:1 17 25 28 22 31 33 13 18 14 18 33 33 28 33 20 25 24 23 24 23

C27:1 3 7 7 11 19 16 16 37 30 37 9 11 17 18 25 31 34 39 38 40

C29:1 1 1 2 4 1 1 3 3 6 6 2 2 1 4 2 3 3 4 3 4

C31:1 3 1 1 2 1 1 1

Blind samplesG

The black dots indicate the blind samples that matched a particular colony based on the rule that the proportion of each 9-alkene was within 5% of the proportion in the colony.

J Chem Ecol (2008) 34:10721080 10751075

delineate the area of the total ion chromatogram for integration. This method introduced some margin of error, but this was expected to be equal across all samples analyzed. In cases in which isomers overlapped completely (e.g., 3,11-diMeC25 and 3,13-diMeC25), peak area was divided according to the ratio in which the diagnostic ions were present.

Method Used to Search for Colony-Specific Signals

All CHC profiles were of two types. Those with limited diversity, comprising hydrocarbons of only one chain length or a short homologous series of hydrocarbons, which were usually dimethylalkanes, and those comprising long homologous series (alkanes, alkenes, and monomethylalkanes) of hydrocarbons. We assumed that the amount of information contained within a homologous series depended on whether or not the ratios (relative amounts) of the individual

compounds were highly correlated (r2>0.9) to each other. For a highly correlated homologous series, we assumed that the information encoded within the entire series was effectively the same as the information encoded in a single compound. We also assumed that a colony signal should be contained only within a homologous series that is highly correlated at the colony and not at the species level. A similar logic can also be applied to isolated compounds. That is, their occurrence and ratio of abundance to each other should be constant within a colony but vary among colonies. Therefore, correlation levels of major CHCs in each homologous series or among isolated compounds were determined at the species and colony level.

Once a group of compounds had been identified as containing potential colony signatures (referred to as signature CHCs), their ability to encode colony-specific information was tested by using two methods. First, one ant was

C21:1

C23:1

C25:1

C27:1

C29:1

C31:1

Percentage of (Z)-9-alkenes

G H B J D I C F A E 8 60 22 56 71 35 64 40 53 69

i iv

iii

Finland (mainland populations) Finland (Island population)

Fig. 2 Relative amounts of various 9-alkenes in Formica exsecta colonies sampled from four mainland locations (i Byvgen, ii Tvarminne, iii

Grkrr, and iv Harparskog) and a single island population in Finland. Standard deviation is shown where it is >1%

1076 J Chem Ecol (2008) 34:10721080

Table3Theaveragepercentages(oftheentirecuticularhydrocarbonprofile)ofnineC 25-dimethylalkanesin30Formicafuscacolonies,basedonn1samples

Colonycode29284015322731351622R135610497100931031069199766164S2470M5M16957

N31033333331033334333353333535533

11,15-DiMeC 25216103323111

9,13-DiMeC 251652112146112112

7,11-DiMeC 252612623

7,15-DiMeC 2512163225

5,13-DiMeC 2523156122365512111681161485

5,15-DiMeC 25417721

5,17-DiMeC 251818282917

3,11-DiMeC 251217

3,13-DiMeC 2554162322199161892111182021201831261624143813105

Blindsamples

R13

104

100

103

J Chem Ecol (2008) 34:10721080 10771077

N31033333331033334333353333535533

106

S24

TheblackdotsindicatetheblindsamplesthatmatchedaparticularcolonybasedontherulethattheproportionsofeachC 25-dimethylalkaneintheblindsamplewaswithin5%oftheproportion

inthecolony.

randomly chosen from each colony, and the proportions of each signature CHC were calculated based on the total relative amount of CHCs in the profile. This was the blind sample. Then, the average proportion of each signature CHC for each colony was calculated from the remaining individuals of a colony. Each blind sample was assigned to the colony or colonies that possessed the same profile (5%) with respect to the signature CHCs. A greater amount of inter-colony variation in signature CHCs was observed in F. fusca than in F. exsecta, and, therefore, there was greater ambiguity in assigning blind samples to a colony for this species. Second, we used hierarchical cluster analysis (Wards method; SPPS v.14) to assign individual ants to a pre-defined number of clusters (colonies) by using the signature proportional data.

Subsequently, the proportions of the signature CHCs were recalculated by ignoring the rest of the profile so that the signature CHCs accounted for 100% of the profile. Although this did not change the overall result, it made the graphical comparisons clearer and may be more biologically relevant, as different groups of hydrocarbons (e.g., alkanes vs. alkenes) are perceived differently (Sachse et al. 1999; Chaline et al. 2005).

Results

Formica exsecta

The CHC profile of F. exsecta was dominated (>95%) by a group of (Z)-9-alkenes and a homologous series of alkanes. In F. exsecta, the alkenes were poorly correlated at the species level but were highly correlated (r2>0.95) at the colony level (Table 1), thus making them prime candidates for encoding colony-specific signals. The variation of the six signature (Z)-9-alkenes across F. exsecta colonies was large (Fig. 1a), especially considering that the average intra-colony variation (SD) in the 20 colonies for all alkenes was small (21%). By using only the proportions of the six signature (Z)-9-alkenes (9-C21:1 to 9-C31:1), all 20 blind

samples were correctly assigned to their colonies (Table 2), although two ants could also each be assigned to another colony that had a similar profile (Table 2). By using the hierarchical cluster analysis, we also correctly assigned 94 of the 97 individuals into the 20 clusters (colonies), with the three incorrectly assigned ants mixed between colonies D and I. Using only the alkanes, 52% (50 out of 97) of the individuals were assigned to their correct colonies. These data support the unique distributions of the (Z)-9-alkenes containing colony-/nest mate-specific information. Although colonies from the various populations may possess similar traits (e.g., the presence of C21:1 in the Byvgen

population), the amount of variation between colonies within each population was striking (Fig. 2).

Table3(continued)

Colonycode29284015322731351622R135610497100931031069199766164S2470M5M16957

1078 J Chem Ecol (2008) 34:10721080

Formica fusca

The CHC profile of 111 F. fusca workers was composed of homologous series of alkanes, monomethylalkanes, and, unusually, a relatively large number of positional isomers of C25dimethylalkanes. All the compounds within each homologous series of alkanes or monomethylalkanes were highly correlated at both the species (r2>0.9) and colony level (r2>0.9), indicating that these compounds probably do not contain colony-specific information. Of the 14 different dimethylalkanes detected in the Finnish population, nine exhibited large amounts of variation when compared to other CHCs (Fig. 2b). The nine positional isomers of dimethyl pentacosane contributed 1537% of the total CHC profile. Each of the 30 colonies possessed two to seven of these nine compounds in a variety of

combinations and proportions. By using only the proportions of these nine signature CHCs, all 30 blind samples were assigned to their correct colonies (Table 3). However, there was some ambiguity in assigning two of these ants due to similarity of profiles with other colonies (Table 3). The hierarchical cluster analysis supported the rule-based analysis by correctly assigning 107 of the 111 individuals into 30 clusters (colonies). The variation of these nine signature C25dimethylalkanes among the 30 F. fusca colonies was clearer when their proportions were analyzed independently from the rest of the CHCs in the profiles (Fig. 3). Despite the large variation (range=094%) of these signature CHCs among colonies (Fig. 3), the intra-colony variation was low within each of the 30 colonies, with the SD averaging only 32% across all signature compounds.

Raseborg Grkrr Hanko Matalan

Bvygen

Santala

Sandbcken

100%

80%

Proportion of C 25-dimethylalkanes

3,11 dimeC25

3,13 dimeC25

5,17 dimeC25

5,15 dimeC25

5,13 dimeC25

7,15 dimeC25

7,11 dimeC25

9,13 dimeC25

11,15 dimeC25

60%

40%

20%

29 3 56

r13

13 5

15 32 27 22

100 103 106 91 99 76

104 97 93 61 64 69

m1 57

s24 70

Colony identification number

Fig. 3 The relative proportions of nine colony-specific C25dimethylalkanes from 30 Finish Formica fusca colonies collected at seven locations. The colonies are grouped within each population according

to the number of C25dimethylalkanes present. The variation is not shown for the sake of clarity, but the SD averaged 32% for all compounds across all the colonies

J Chem Ecol (2008) 34:10721080 10791079

Discussion

It has been suggested recently that the information encoded within CHC profiles, which social insects use to discriminate between nest mates and non-nest mates, resembles a blurred barcode (Boomsma and Franks 2006). However, we have shown in this study that colony-specific information can be encoded in the CHC profile in two distinct ways, both of which are clear and distinct once identified from the rest of the CHC profile.

Mechanism 1: Altering the Proportions of a Single Type of Hydrocarbon (F. exsecta)

Despite F. exsecta possessing one of the most basic CHC profiles among the Formica ants, it encodes colony-specific information in the proportions of individual hydrocarbons within a single homologous series (of 9-alkenes). Such encoding presumably requires precise control during each step of the chain-lengthening process or in the lipophorin transport system (Schal et al. 2001; Lucas et al. 2004). The encoding of information in a single homologous series of hydrocarbons limits the number of possible unique signatures across colonies. Despite this, F. exsecta populations are able to produce a wide variety of distinct colony-specific distributions of alkenes (Fig. 3). Recent experimental evidence (Martin et al. 2008a) with synthetic CHCs has shown that F. exsecta uses (Z)-9-alkenes to encode nest-mate recognition signals. Our interpretation is supported by data on F. japonica in Japan (Akino et al. 2004), which has a similar CHC profile to F. exsecta. When synthetic CHCs (9-alkenes and alkanes) were placed on a glass dummy in proportions that mimic a particular colony, F. japonica nest mates were not aggressive and non-nest mates were aggressive toward the dummy in the two colonies tested.

Mechanism 2: Synthesis of Colony-specific Compounds (F. fusca)

A review of the CHC literature shows that dimethylalkanes in a given species are synthesized principally in one-carbon chain length, as found in F. fusca or in limited homologous series (Howard and Blomquist 2005). If only the presence or absence of the nine C25dimethylalkanes found in

F. fusca encoded a colony signature, then 512 (29) unique colony signatures could exist. Among the 30 colonies studied, 24 unique profiles were found based on combinations of presence or absence of specific compounds, thus illustrating the diverse production of CHC profiles within this species. However, the proportions of each C25

dimethylalkane also varied between colonies, potentially increasing the number of unique colony profiles (e.g., up to

109 if a 10% discrimination window is used) dramatically. Behavioral work is needed to determine what differences in a given CHC profile are allowable before it is no longer recognized as that of a nest mate.

The role of methyl-branched hydrocarbons in nest-mate recognition has been implicated in Polistes wasps (Dani et al. 2001) and the ants Camponotus vagus (Clement et al. 1987), Messor barbarus (Provost et al. 1994), possibly Cataglyphis spp (Dahbi et al. 1996), and now F. fusca (this study). However, in all these studies, including this one, bioassays that use synthetic methyl-branched hydrocarbons have yet to be conducted. This work needs to be carried out to confirm that these compounds are indeed used in nest-mate recognition. From an evolutionary perspective, dimethylalkanes are ideally suited to function as communication molecules because there are numerous isomers for a given chain length, and a relatively minor chemical change, such as in position of a methyl group, can have a profound effect on the conformation of the molecule. This may explain why dimethylalkanes are by far the most diverse type of hydrocarbon found among the ants (Dahbi et al. 1996).

The two systems described here or variations of them may be expected to occur in many species of social insects that have strong colony identity. We believe that the addressing of the roles of chain length, detection thresholds, and biosynthesis in social insect CHCs will provide insight into the world of insect communication and the role of nest-mate recognition in the evolution of sociality.

Acknowledgment Many thanks go to Liselotte Sundstrm of Helsinki University for assistance with the field work, Jennifer Aldworth of Keele University in helping with the DMDS reactions, Duncan Jackson of Sheffield University for his critical reading of earlier drafts, and many colleagues for their constructive comments, especially David Morgan of Keele University. Funding for this research was provided by NERC (NE/C512310/1) and Academy of Finland grants (213821 and 206505).

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Colony-specific Hydrocarbons Identify Nest Mates in Two Species of Formica Ant

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