cuticular hydrocarbons in two parapatric species of ants and their hybrid

259© 2011 ISZS, Blackwell Publishing and IOZ/CAS

ORIGINAL ARTICLE

Cuticular hydrocarbons in two parapatric species of ants and

their hybrid

Mohamed EL-SHEHABY,1,2

Mohamed Sayed SALAMA,2

Elisabeth BRUNNER1

and Jürgen

HEINZE1

1Biologie I, University of Regensburg, Regensburg, Germany and

2Department of Entomology, Ain Shams University, Cairo, Egypt

Abstract

Discrimination between nestmates and non-nestmates in social insects is thought to rely on the pattern of cuticular

hydrocarbons. We investigated the cuticular hydrocarbon profiles of 2 parapatric sibling ant species, Temnothorax

nylanderi (Förster, 1850) and Temnothorax crassispinus (Karavaiev, 1926), and their hybrid. We found that although

the profiles show considerable similarities, a discriminant analysis based on the relative peak areas of cuticular hydro-

carbons separates the 3 taxa. The profiles of hybrids were not consistently intermediate between those of the paternal

species, suggesting either non-additive interactions among the parental biosynthetic pathways or systematic differ-

ences in environment-derived odor cues.

Key words: colony odor, cuticular hydrocarbons, hybridization, Temnothorax.

Correspondence: Mohamed El-Shehaby, Universität Regensburg,

Universitätsstraße 31, 93040, Regensburg. Germany.

Email: [email protected]

INTRODUCTION

Hybridization appears to be a rather common phenom-

enon in ants. It has been suggested that in some species, a

considerable percentage of female sexuals mate with a

male from a different species (Seifert 1999; Seifert &

Goropashnaya 2004; Nonacs 2006). Although in numer-

ous cases, hybrid queens are not fertile themselves, hy-

bridization in ants might be selected against less strongly

than in other species, because hybrid workers are often

viable and can rear the haploid; that is, the pure-bred male

offspring of the mother queen (Seifert 2006; Umphrey

2006; Feldhaar et al. 2008). Furthermore, mating with a

wrong partner could have a negligible effect when female

sexuals mate with multiple males. In Pogonomyrmex har-

vester ants, regular mating of queens with both conspe-

cific and heterospecific males might even have led to the

evolution of genetic caste determination with pure-bred

female sexuals and hybrid workers (e.g. Helms Cahan &

Keller 2003). Although several studies have investigated

the morphology of hybrids, little is known about their

behavior, the stability of their colonies and their commu-

nication (but see Kulmuni et al. 2010).

Of special interest is the effect of hybridization on

nestmate recognition cues. Insect societies are usually closed

systems, from which unrelated intruders are excluded

through a sophisticated system of nestmate discrimination

(e.g. Hölldobler & Wilson 1990). There is growing evidence

that surface lipids, in particular cuticular hydrocarbons, play

an important role in the distinction between friends and foes

in insect societies (e.g. Singer 1998; Howard & Blomquist

2005; Nehring et al. 2010). Linear and branched, long-

chained alkanes and alkenes make up a large part of the

cuticular waxes of insects (e.g. Martin & Drijfhout 2009)

and serve in water-proofing the cuticula (e.g. Gibbs 1998;

Howard & Blomquist 2005). The enormous variation of

Integrative Zoology 2011; 6: 259-265 doi: 10.1111/j.1749-4877.2011.00255.x

260 © 2011 ISZS, Blackwell Publishing and IOZ/CAS

cuticular blends both within and between colonies has long

suggested that, in addition, they play an important role in

communicating an individual’s sex, task, age, fecundity,

species and colony of origin. This is clearly evidenced by

the reaction of social insects to artificial or manipulated

mixtures of cuticular hydrocarbons applied to the surface of

other individuals (e.g. Lahav et al. 1999; Akino et al. 2004;

van Wilgenburg et al. 2010). Discrimination cues appear to

be in part derived from the environment and in part heri-

table (e.g. Liang & Silverman 2000; van Zweden et al. 2009),

and the influence of nature and nurture varies considerably

among species. Investigating the cuticular profiles of hy-

brids might help to quantify the influence of genes and en-

vironment on colony odor. In fire ants, hybrids of Solenopsis

invicta and Solenopsis richteri were more aggressive towards

conspecific non-nestmates than either parental species, prob-

ably because of a higher variability of heritable recognition

cues (Obin & Vander Meer 1989). The cuticular hydrocar-

bons of the hybrid appeared to be a mixture of the parental

bouquets (Vander Meer et al. 1985).

The 2 sibling species Temnothorax nylanderi (Förster,

1850) and Temnothorax crassispinus (Karavaiev, 1926)

are among the most common ant species in deciduous

forests throughout Central Europe (Buschinger 1968; Pla-

teaux 1970; Foitzik & Heinze 1998; Strätz & Heinze

2004). Their colonies consist of only a few dozen indi-

viduals and usually a single queen. They live in small cavi-

ties in plant material, such as hollow acorns, in rotting

twigs or under bark. The 2 species are parapatrically dis-

tributed and form a narrow hybrid zone where they meet

(Seifert 1995; Pusch et al. 2006a,b).

Here, we complement previous research on the chemi-

cal ecology of Temnothorax ants through a comparative

analysis of the cuticular hydrocarbon patterns of T.

nylanderi, T. crassispinus, and their hybrid from a popu-

lation in Franconian Jura near Velburg, where populations

of the 2 parental species are separated only by a few hun-

dred meters of agricultural land.

MATERIALS AND METHODS

Temnothorax nylanderi and T. crassispinus are morpho-

logically very similar but can be distinguished quite easily

by electrophoresis of the enzyme glucose-6-phosphate

isomerase (GPI; P. Douwes, cited in Seifert 1995). Almost

all investigated T. crassispinus workers are homozygous for

an electromorph with medium electrophoretic migration

velocity (m), whereas most T. nylanderi are homozygous

for a fast electromorph (f) (Pusch et al. 2006a,b). Hybrids,

which occasionally occur in the contact zone, show the het-

erozygote genotype mf (Seifert 1995; Pusch et al. 2006a,b).

In April 2009, we collected complete colonies of the 2

species and their hybrid by searching potential nest sites

in oak, pine and beech forests near Velburg in the

Franconian Jura. We focused fieldwork on 3 previously

studied areas: Schlossberg, 49°14’N (site 1), 11°38’E and

2 sites at Eichelberg (49°14’N, 11°39’E, sites 2 and 3).

Immediately after collection, all colonies were censused

and frozen at –20 °C.

For species determination, we analyzed the GPI

electromorph of 5 ants per colony by polyacrylamid gel

electrophoresis, as described in Pusch et al. (2006a,b).

Electromorphs were named according to their electro-

phoretic migration velocities (f, fast; m, medium; s, slow;

Pusch et al. 2006a,b). Colonies were categorized as T.

crassispinus, T. nylanderi or hybrid, when all genotyped

individuals were homozygous mm, ff, or heterozygous mf,

respectively.

Cuticular hydrocarbons were extracted from 18 workers

of T. crassispinus from 8 colonies (site 3), 9 T. nylanderi

workers from 3 colonies (site 1), and 9 hybrid workers from

4 colonies (site 2) by solid phase microextraction, as de-

scribed previously (e.g. Brunner et al. 2009). A 30 µm

polydimethylsiloxane fiber A was gently rubbed for 10 min

against the gaster of the ant and thereafter inserted into the

injection port of an Agilent Technologies 6890N gas chro-

matograph equipped with a flame ionization detector and a

HP-5 capillary column (30 m ! 0.32 mm ! 0.25 µm; J&W

Scientific, USA). The injector was split/splitless and the

carrying gas was Helium at 1 mL/min. The temperature was

initially held at 70 °C for 1 min, increased from 70 °C to

180 °C at 30 °C/min, from 180 °C to 310 °C at 5 °C/min,

and held constant at 310 °C for 5 min. As solid-phase

microextraction does not allow the usage of an internal standard,

we used 3 external standards (n-C21

, n-C25

and n-C26

). To

identify peaks, we compared the chromatograms with re-

sults from other studies on T. nylanderi and T. crassispinus,

in which substances had been identified by mass spectrom-

etry (e.g. Brunner et al. 2011).

In total, gas chromatography analysis gave 83 peaks.

For statistical analyses we used the standardized areas of

42 peaks consistently present in all 3 types (see also

Brunner et al. 2011). Peak areas were transformed by us-

ing the formula: Zij = log[Xi,j/g(Xj)], with Xi,j being the

standardized peak area i for the sample j, and g(Xj) the

geometric mean of all peaks of the sample j (Reyment

1989). To reduce the number of variables for multivariate

statistics we analyzed these data by principle component

analysis (PCA) and used the obtained factors in a discrimi-

nant analyses (DA) to determine whether hydrocarbon

profiles separated reliably among species. Due to techni-

M. El-Shehaby et al.


cal problems, the number of samples was very limited. It

is advised to perform DA with at most n-2 independent

variables if the smallest sample size is n (e.g. McGarigal

et al. 2000). Therefore, in our DA, we used the 4 factors

with the largest eigenvalues.

We used Mann-Whitney U-tests to compare percent-

ages of single compounds between groups and adjusted

p-values for multiple comparisons, as suggested by

Benjamini & Hochberg (1995). Statistical analysis was

performed using Statistica 6.0.

RESULTS

In agreement with previous studies (Pusch et al. 2006b),

colonies were mostly T. nylanderi at site 1 (15 colonies

with genotype ff, 1 colony mm and 1 colony fs) and mostly

T. crassispinus and hybrids at sites 2 (1 colony ff, 12 colo-

nies mm and 4 colonies mf) and 3 (34 colonies mm and 4

colonies mf).

The cuticular bouquet of Temnothorax workers is char-

acterized by linear and methyl-branched alkanes with chain

lengths ranging from C25

to C33

. With our equipment we

cannot exclude the presence of substances with longer chain

lengths (e.g. Martin & Drijfhout 2009). Of the 42 peaks used

for the statistical analyses, 8 represented linear alkanes, 22

were single or mixtures of branched alkanes, and 10 were

dimethyl alkanes. The remaining 2 substances could not be

identified. PCA based on the peak areas gave 12 factors with

eigenvalues larger than 1, which in total explained 88.3% of

the variance. The 4 largest factors with eigenvalues >3 ex-

plained a total of 58.3% of the variance.

Discriminant analysis based on the 4 largest factors sepa-

rated between the 3 taxa (Wilks’ = 0.311, F8,60

= 5.943,

P < 0.001; Fig. 1) and almost all individuals were cor-

rectly classified (T. crassispinus 15 of 18; T. nylanderi 8

of 9; hybrids all 9; overall correct classification 88.89%).

Squared Mahalanobis distances were all highly signifi-

cant (T. nylanderi – T. crassispinus 4.839, P = 0.0012;

T. nylanderi – hybrid: 6.646, P = 0.0011; T. crassispinus

– hybrid: 4.526, P = <0.0017). The parent species differed

considerably in the proportions of 12 substances (in

particular, n-C26

, 3-me C28

, and 5-me C29

, Mann–Whitney

U-tests, P < 0.05; after correction for multiple testing using

the Benjamini-Hochberg method, none of the 42 differences

is stil l significant at the 5% level, but 11 differences are still

significant at the 10% level). The hybrid differed in the pro-

portions of 9 substances from T. crassispinus (of which the

proportions of x,y dime-C29

, 13,17 dime-C31

,

3,x dime-C33

,

3,7 dime-C27

and an unidentified substance were significantly

different at the 5% level

after correction) and in the propor-

tions of 13 substances from T. nylanderi (of which 11, in-

cluding 3-me C28

, n-C28

, 5-me C29

and 3,7 dime-C27

, were

significant at the 10 % level after correction; Table 1). In

contrast to what might be expected, the proportions in the

hybrids were not always intermediate between those from

the parental species. For example, hybrids had a significantly

higher proportion of 3,7 dime-C27

and x,y dime-C29

than

either of the parental species (Fig. 2).

Figure 1 Scatter plot of the canonical

scores for pairs of discriminant functions

(canonical roots) based on an analysis of

standardized peak areas of cuticular hydro-

carbons of the ants Temnothorax nylanderi,

T. crassispinus and their hybrid.

Colony odor in a hybrid ant


DISCUSSION

The parapatric sibling species T. nylanderi and T.

crassispinus are extremely similar in their morphology, ecol-

ogy and behavior. They are also very similar in their cuticu-

lar hydrocarbon profiles; that is, the quantitative and quali-

tative composition of linear and branched alkanes and alk-

enes that is believed to convey the information ants and other

social insects utilize in nestmate discrimination.

Nevertheless, previous gas chromatographic studies have

documented subtle, but statistically significant differences

between the 2 species (e.g. Foitzik et al. 2007; Brunner

et al. 2011). This is also corroborated by our analysis, in

that a discriminant analysis based on standardized peak

areas of cuticular hydrocarbons correctly assigned most

individuals according to species. Surprisingly, hybrids be-

tween the 2 species were also accurately classified, sug-

gesting that hybridization results in a third specific cu-

ticular profile. It must be cautioned, however, that our

study relies on a very limited number of individuals from

only a few colonies and our conclusions, therefore, need

to be considered as preliminary. Research with additional

material, correction for variation among colonies and col-

lecting sites, and the inclusion of hydrocarbons with longer

change lengths might change this picture.

In contrast to what has been observed in studies on

Solenopsis fire ants and their hybrid (Vander Meer et al.

1985), the proportions of individual cuticular substances in

T. nylanderi ! T. crassispinus hybrids did not consistently

fall in between the proportions of the parental species. This

might reflect complex interactions among the biosynthetic

pathways inherited from the 2 parents, as has been shown in

hybrid plants (Orians 2000). For example, an elongase from

1 species combined with a methylase from the other might

yield hydrocarbons in the hybrid that are not present in the

parental species. In addition, small differences between

heritable, species-specific profiles might have been inflated

by systematic environmental differences among the 3 sites

at which the 3 different taxa were collected. Previous stud-

ies have indicated the importance of environment-derived

odor cues for nestmate recognition in the parental species.

Workers from different colonies cease to interact aggres-

sively within a few days of standardized culture in the labo-

ratory (Heinze et al. 1996), and the chemical bouquet of T.

crassispinus colonies quickly changes during laboratory

culture and loses its colony specificity (M. El-Shehaby,

unpubl. data). Neighboring, conspecific colonies, which pre-

sumably utilize similar food sources and nest material,

readily fuse in the field (Foitzik & Heinze 1998; Tichá 2002),

and colonies of T. nylanderi and T. crassispinus have been

observed to do so at least in the laboratory (Pusch et al.

2006c). In our study site, populations of the 2 parental spe-

cies are not syntopic, but occur in 2 superficially identical

patches of deciduous forest, which are separated by a 500m

wide strip of agricultural land. Hybrids occur only at the

westernmost edge of the eastern forest, which is otherwise

populated only by T. crassispinus. Future studies shall re-

veal whether differences in local environmental conditions

or non-additive genetic interactions underlie the non-inter-

mediate hydrocarbon profiles in hybrids.



Table 1 Differences in the abundance of particular hydrocarbons on the cuticles of the ants Temnothorax nylanderi, Temnothorax

crassispinus and their hybrid

*Significant at 0.05 level after correction for 42 tests. †Marginally significant at the 0.1 level after correction for 42 tests.




Assuming that sexuals locate and identify suitable mates

by their cuticular hydrocarbons in addition to glandular sub-

stances (e.g. Ayasse et al. 2001; Beibl et al. 2007), the regu-

lar occurrence of hybrids in the field might mean that the

odor differences between the 2 parental species are not suf-

ficient to maintain prezygotic reproductive isolation. Mito-

chondrial DNA (mtDNA) data indicate that T. nylanderi

and T. crassispinus diverged 1.5–2 Ma (Pusch et al. 2006a),

and as yet there is no firm evidence for the occurrence of

fertile hybrid queens in our study site (Pusch et al. 2006a,b).

Therefore, hybridization between the 2 species is an evolu-

tionary dead end and one might wonder why the odor cues

of the 2 species have not yet diverged more. Studies in other

insects, such as fruit flies and crickets, suggest a rapid di-

versification of cuticular hydrocarbon bouquets and char-

acter displacement when related taxa occur in sympatry

(Higgie et al. 2000; Mullen et al. 2007). The answer to this

problem might have 2 parts. First, as mentioned above, hy-

bridization in haplodiploids is associated with lower costs

as mothers still can rear sons from unfertilized eggs (Seifert

2006; Umphrey 2006; Feldhaar et al. 2008). Second, the 2

species immigrated into Central Europe only after the last

glaciations and their ranges are still expanding (Pusch et al.

2006a). Hybrid zones probably formed only a few hundred

generations ago and the time since the secondary contact

between the 2 species might not have been sufficient to se-

lect against allospecific mating.

ACKNOWLEDGMENTS

This project was carried out with permission from Al-

Azhar University, Cairo and the Ministry of High Educa-

tion of the Arab Republic of Egypt, and supported by funds

from the Deutsche Forschungsgemeinschaft. Andreas

Trindl, Jan Oettler and Tina Wanke helped to collect colo-

nies and Jürgen Trettin assisted with allozyme analysis

and Doris Rothgänger with gas chromatography. We thank

the referees for helpful comments on the manuscript.

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cuticular hydrocarbons in two parapatric species of ants and their hybrid

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