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Myrmecological News 15 109-115 Vienna, May 2011 Mating, hybridisation and introgression in Lasius ants (Hymenoptera: Formicidae) Tom M. VAN DER HAVE, Jes Søe PEDERSEN & Jacobus J. BOOMSMA Abstract Recent reviews have shown that hybridisation among ant species is likely to be more common than previously appreci- ated, but that documented cases of introgression remain rare. After molecular phylogenetic work had shown that Euro- pean Lasius niger (LINNAEUS, 1758) and L. psammophilus SEIFERT, 1992 (formerly L. alienus (FOERSTER, 1850)) are unlikely to be very closely related, we decided to analyse an old data set confirming the conclusion by PEARSON (1983) that these two ants can indeed form viable hybrids. We show that signatures of introgression can be detected in a Danish site and that interspecific gene-flow is asymmetrical (only from L. niger into L. psammophilus) as inferred previously by Pearson for the southern England site that he studied and from which we also collected data. We compare the ob- served patterns of hybridisation and introgression in the Danish and British site and infer that overlap in nuptial flights in Denmark may have contributed to the higher frequency of introgressed genes relative to the southern England site where nuptial flights are clearly separated in time. We also report the first mating system data for L. psammophilus, showing that this species has facultative multiple mating of queens similar to L. niger. We suggest that L. psammophilus- niger introgression may be much more common than previously appreciated, which would explain that European myr- mecologists have often found it difficult to distinguish between these species at sites where they occur sympatrically. This would imply that multiple accessible field sites are available to study the molecular details of hybridisation and in- trogression between two ant species that have variable degrees of sympatry throughout their distributional ranges. Key words: Allozymes, relatedness, paternity, mating frequency, heath land, Hartland Moor, Mols Bjerge. Myrmecol. News 15: 109-115 (online 20 April 2011) ISSN 1994-4136 (print), ISSN 1997-3500 (online) Received 12 October 2010; revision received 7 March 2011; accepted 8 March 2011 Dr. Tom M. van der Have, Department of Plant Ecology and Evolutionary Biology, Utrecht University, Padualaan 8, NL-3584 CH Utrecht, The Netherlands. Present address: Resource Ecology Group, Wageningen University, Droeven- daalsesteeg 3a, NL-6708 PD Wageningen, The Netherlands. E-mail: [email protected] Assoc. Prof. Dr. Jes Søe Pedersen & Prof. Dr. Jacobus J. Boomsma (contact author), Centre for Social Evolution, De- partment of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark. E-mail: [email protected]; [email protected] Introduction It is only a decade ago that hybridisation between ant spe- mating systems. The most recent examples are studies in cies was considered to be rare, but this notion was changed Formica wood ants documenting segregation distortion when SEIFERT (1999) compiled evidence that over 10% of leading to large scale differentiation between male and fe- the central European ants may occasionally hybridise and male genomes of the same species (KULMUNI & al. 2010) that strong evidence for this phenomenon was already avail- and the convergent appearance of multiple hybridisation able for Leptothorax albipennis (CURTIS, 1854) (now Tem- events between the same pair of species (SEIFERT & al. nothorax albipennis) and Lasius jensi SEIFERT, 1982. A few 2010). years later the journal Ecology published a special feature Some of the first studies combining morphology and issue on the ecology and evolution of hybridisation in ants genetic marker techniques to elucidate hybridisation were (NONACS 2006), focusing mostly on Pogonomyrmex har- done by PEARSON (1982, 1983), showing that sympatric vester ants where it had become clear that in some species Lasius niger (LINNAEUS, 1758) and L. "alienus" (FOERS- workers arise from hybrid matings whereas gynes produced TER, 1850) occasionally form F1 hybrids at Hartland heath in the same colonies are pure bred (LINKSVAYER & al. in Dorset, UK and that this hybridisation appeared to be 2006). More recent studies further showed that ant species restricted to L. alienus queens mating with L. niger males. may have very bizarre breeding systems with different gen- At that time, however, the taxonomy of the subgenus La- etic pathways towards producing males, gynes and wor- sius s.str., to which these species belong, was so confus- kers (reviewed by FELDHAAR & al. 2008). This corrobor- ing that these species were generally considered to be each ated the notion that many such cases may have been over- other's closest relatives (i.e., sister species, although this looked and that explicit genetic studies of hybridisation term was hardly used in the 1980s). The taxonomy of La- and introgression have the potential to provide important sius was completely revised by SEIFERT (1992), who de- insights in the evolutionary potential of ant breeding and scribed several new species and renamed others, among Ross H. Crozier Memorial Volume them sandy-heath-land L. alienus, which became L. psam- usually warm, humid and with little wind, when alates dis- mophilus SEIFERT, 1992. However, it was only after the pub- persed synchronously over relatively large areas (BOOMS- lication of the first Lasius phylogeny (STEINER & al. 2004) MA & LEUSINK 1981). that it became clear that L. niger and L. psammophilus Collection dates for newly inseminated Lasius niger were less closely related than previously assumed, which queens were 8 August 1984 (Hartland) and 15 August 1985 implied that the possibility of hybridisation and asymme- (Mols), and 18 (evening) to 19 (early morning) August 1985 tric introgression between these two species became more (Mols) for L. psammophilus. Queens were stored together interesting. in trays at 5°C and high relative humidity for up to four Two of us (TMvdH and JJB) had the opportunity to ini- months before they were set up individually in 20 ml pots tiate follow-up studies of PEARSON (1982, 1983) in the sec- with a small sponge that was watered twice a week (for ond half of the 1980s, both at the Hartland population in further details see BOOMSMA & ISAAKS 1982, BOOMSMA Dorset and in a similar population at Mols, Denmark, where & VAN DER HAVE 1998). Queen mortality was low during worker morphology of sympatric Lasius niger and L. psam- the months of artificial hibernation and moderate during the mophilus (hair numbers on tibia and scapus) was so vari- individual rearing period (27% in L. psammophilus, Mols, able that hybridisation was suspected (M.G. Nielsen, pers. to 29% in L. niger, Mols), probably not exceeding normal comm). However, although presented at the 1986 IUSSI mortality under field conditions. Queens produced their first congress in Munich (VAN DER HAVE 1987), this work was batch of three to ca. 20 workers after two to four months, never published, except for some of the L. niger data on after which they were frozen and either analysed directly multiple queen mating, which were used in a comparative or stored at -70°C for later allozyme analysis. analysis of the variation in queen mating frequencies among Allozyme genotypes were obtained by horizontal starch L. niger populations in Northwest (NW) Europe (BOOMSMA gel electrophoresis of males, gynes (virgin queens) and & VAN DER HAVE 1998). workers sampled from the field colonies and from the In the present paper we present both the hybridisation queens and workers of the incipient colonies. Allele fre- and the queen mating data that we obtained from the Hart- quencies across field colonies were calculated from infer- land and Mols populations of Lasius niger and L. psam- red maternal queen genotypes, whereas they could be ob- mophilus. The hybridisation data confirm that the two spe- tained directly from queens of the incipient colonies, except cies also hybridise in the Danish site and that clear indica- for Lasius psammophilus at Hartland, where flights were tions for asymmetric introgression can be found. The mat- observed but no newly inseminated queens could be col- ing system data show that L. psammophilus has facultative lected. These comparisons were subsequently used to esti- multiple mating of queens, similar to L. niger, confirming mate the number of males that queens had mated with (mat- the general notion that eusocial insect species of the same ing frequencies) using up to three informative and genetical- (sub)genus normally have very similar mating systems ly variable loci (Malate dehydrogenase [Mdh-1], Esterase-2 (BOOMSMA & RATNIEKS 1996, BOOMSMA & al. 2009). [Est-2] and Malic enzyme [Me]), which segregated three However, we used a more sophisticated technique for esti- (Mdh-1) to five (Est-2) alleles. Details of the electrophore- mating queen mating frequency (PEDERSEN & BOOMSMA sis procedure are given by VAN DER HAVE & al. (1988). 1999) compared to the reanalyses of literature data pro- A total of 105 field colonies and 276 mother-offspring com- vided by BOOMSMA & RATNIEKS (1996), confirming the binations were analysed, involving 1956 workers from new- prediction of PEDERSEN & BOOMSMA (1999) that the older ly inseminated queens and 1355 workers, 316 gynes and statistical techniques tended to underestimate the frequency 987 males from mature field colonies. Samples of workers of multiply mated queens. and gynes were pooled for further analysis to maximise sam- ple size of female offspring per colony and hence improve Materials and methods accuracy of mating frequency and relatedness estimates. Lasius niger and L. psammophilus populations in both Eng- We used the method developed by PEDERSEN & BOOMS- land and Denmark were observed intensively during the MA (1999) as implemented in the program MATESOFT 1.0 period of nuptial flights to study interspecific mating oppor- (MOILANEN & al. 2004) to assign female offspring (workers tunities and to collect inseminated gynes shortly after their and gynes) to patrilines and to correct estimates of the pro- nuptial flight.