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The Coexistence Myrmecological News 18 25-32 Vienna, March 2013 Mating system and population genetic structure of the bulldog ant Myrmecia pavida (Hymenoptera: Formicidae) Paula CHAPPELL, Katherine ROBERTS, Boris BAER & William O.H. HUGHES Abstract Understanding the evolution of the alternative mating strategies of monandry and polyandry is a fundamental problem in evolutionary biology because of the cost-benefit trade-offs associated with mating for females. The problem is parti- cularly intriguing in the social insects because queens in most species appear to be obligately monandrous (i.e., only a single male fathers their offspring), while those in a minority of species have evolved high, and sometimes extreme, poly- andry. One group which may shed particular insight is the ant subfamily Myrmeciinae (Myrmecia and Nothomyrmecia). Here we examine the population and colony genetic structure of the bulldog ant Myrmecia pavida CLARK, 1951 by geno- typing offspring workers from 45 colonies. We find little evidence of geographic structuring or inbreeding in the popu- lation, indicating that the species outbreeds, most probably in mating swarms. We also find that queens of M. pavida show moderately high polyandry, with 84% having mated with between two and seven males, and an overall mean ob- served mating frequency of 3.8. This is significantly higher than previously reported for queens of Nothomyrmecia macrops, in which most females mate singly. This was similar to that of M. pyriformis, M. brevinoda, and M. pilosula, the three congenerics for which mating frequencies have recently been reported. The two genera in the Myrmeciinae therefore appear to show multiple transitions in mating frequency and further investigation of the subfamily may be highly infor- mative for disentangling the forces driving the evolution of alternative mating strategies. Key words: Polyandry, monandry, social insect, mating frequency, paternity. Myrmecol. News 18: 25-32 (online 4 December 2012) ISSN 1994-4136 (print), ISSN 1997-3500 (online) Received 13 January 2012; revision received 7 July 2012; accepted 12 July 2012 Subject Editor: Helge Schlüns Paula Chappell, Katherine Roberts & William O.H. Hughes (contact author), Institute of Integrative and Comparative Biology, University of Leeds, Leeds, LS2 9JT, UK. E-mail: [email protected] Boris Baer, Centre for Integrative Bee Research, ARC CoE Plant Energy Biology,University of Western Australia, WA 6009, Crawley, Australia. Introduction Understanding the selective forces that shape different mat- fits in many animals makes it hard to disentangle their re- ing strategies is a fundamental problem that is essential for lative importance. The fact that the costs of polyandry will understanding the evolutionary interplay between natural also vary between taxa makes it additionally difficult to de- and sexual selection, as well as speciation. The occurrence termine whether greater benefits or reduced costs are driv- of monandry and polyandry in different taxa remains a ing the evolution of higher mating frequencies in specific conundrum in evolutionary biology. Monandry (females taxa. The occurrence of polyandry is in addition of parti- each being fertilised by only a single male) is relatively rare cular interest because it results in significant potential for and females of most animal species are polyandrous (fe- postcopulatory sexual selection, as well as for evolutionary males each being fertilised by multiple males; ARNQVIST & conflicts within and between the sexes (BAER 2011). NILSSON 2000, JENNIONS & PETRIE 2000, SIMMONS 2001, The eusocial Hymenoptera (all ants, some bees and ZEH & ZEH 2003). Polyandry involves greater exposure to some wasps) have proved useful models for understanding the costs of mating, such as sexually transmitted diseases, the evolution of mating strategies. Polyandry reduces the vulnerability to predators, energetic expenditure and risk of indirect fitness benefits which select for social behaviour direct harm by males (CHAPMAN & al. 1995, MAKLAKOV through kin selection (HAMILTON 1964, BOOMSMA 2007). & al. 2005, BAER & al. 2006, MCNAMARA & al. 2008). Accordingly, and in contrast to most animals, the reproduc- However, polyandry can also provide significant benefits tive females (queens) in most eusocial insects are exclu- to females. These may include direct material benefits, such sively monandrous, with polyandry being a derived state as increased sperm, nuptial gifts or paternal care, or indi- (HUGHES & al. 2008a). The costs of polyandry in most spe- rect genetic benefits, such as diluting genetically incom- cies are also likely to be relatively high, because the mat- patible matings or increasing offspring genetic diversity as ing period is one of the riskiest parts of a queen's life as she a bet-hedge against an unpredictable environment (ARN- is not protected by workers (CROZIER & FJERDINGSTAD QVIST & NILSSON 2000, JENNIONS & PETRIE 2000, SIM- 2001, SUMNER & al. 2004, BAER & al. 2006). Nevertheless, MONS 2005). The co-occurrence of direct and indirect bene- approximately a third of social Hymenoptera have evolved facultative, low levels of polyandry (queens being ferti- or departing the nest were collected and stored immedi- lised occasionally by two or three males) and nine clades ately in 100% ethanol. Three morphs were identified based have evolved higher levels of polyandry (> 90% of queens on colouration patterns that differed clearly and consist- being inseminated by multiple males, with the number of ently between nests, with workers within a nest always be- males also often being higher; honeybees, Vespula yellow- longing to the same morph. Morph 1 was found mainly to jacket wasps, army ants, leaf-cutting ants, Pogonomyrmex the west of Perth (28 out of 29 nests), while the only nest of harvester ants, Cataglyphis desert ants, Pachycondyla pone- morph 2 and most nests of morph 3 (15 out of 16 nests) rine ants, and Plagiolepis and Cardiocondyla ants; HUGHES were collected to the east of Perth. All specimens were & al. 2008a, HUGHES & al. 2008b). Polyandry has almost identified by Dr. Steve Shattuck of the Entomology Divi- certainly not evolved in these taxa for direct, material bene- sion of the Australian National Insect Collection (CSIRO) fits because males do not provide paternal care or nuptial as belonging to the species Myrmecia pavida (Hymeno- gifts, do not force females to mate multiply, and multiple ptera, Formicidae, Myrmeciinae). mating does not result in females storing significantly great- DNA sequences for the 28S rRNA gene (28S, 622 bp) er quantities of sperm (FJERDINGSTAD & BOOMSMA 1998, and the Long Wave Opsin gene (OP, 1640 bp) from two CROZIER & FJERDINGSTAD 2001, SCHLÜNS & al. 2005). randomly selected individuals of each of the morphs were However, empirical studies with social insects have pro- produced using primers and protocols as in HASEGAWA duced some of the strongest evidence for females instead & CROZIER (2006) and compared with published sequen- gaining genetic benefits from polyandry, including by di- ces for Myrmecia species (GenBank accession numbers luting genetically incompatible matings and increasing off- AB208449 to AB208482 and AB207106 to AB207135). As spring genetic diversity (BAER & SCHMID-HEMPEL 1999, the sequences from individuals belonging to each morph COLE & WIERNASZ 1999, TARPY & PAGE 2002, CAHAN were identical, and considering the characteristics of the & KELLER 2003, HUGHES & BOOMSMA 2004, JONES & al. genes used (HASEGAWA & CROZIER 2006), no further indi- 2004, HUGHES & BOOMSMA 2006, GOODISMAN & al. viduals were sequenced. A phylogenetic reconstruction us- 2007, MATTILA & SEELEY 2007, SEELEY & TARPY 2007, ing Maximum Parsimony (bootstrap consensus tree, 1000 SCHWANDER & KELLER 2008, WADDINGTION & al. 2010, replicates) was produced using the combined data (28S + CONSTANT & al. 2012). OP = 2262 bp) for each morph, plus 19 other Myrmecia One group of social insects which may be particularly species for which the sequences of the two genes were informative for understanding the evolution of alternative available and Nothomyrmecia macrops as the outgroup. mating strategies is the Australasian ant subfamily Myrme- Pairwise genetic distances (number of base substitutions ciinae. It currently contains 90 described species of the in- per site) among species belonging to the M. gulosa group famous Myrmecia bulldog ants that are classified into nine were calculated in MEGA 4 (TAMURA & al. 2007) using species groups and are conspicuous components of most the Maximum Composite Likelihood method in order to Australian ecosystems, as well as the "living fossil" ant assess if the three morphs could be considered different Nothomyrmecia macrops, which is the only extant member taxa. of its genus (TAYLOR 1978, OGATA & TAYLOR 1991, BOL- Genotyping TON & al. 2007). The subfamily is located in a key, under- studied region of the ant phylogeny and is basal to the vast Microsatellite loci developed for Nothomyrmecia macrops majority of ants for which mating strategies are known (see SANETRA & CROZIER 2000) and Platythyrea punctata (BRADY & al. 2006, MOREAU & al. 2006, RABELING & al. (see SCHILDER & al. 1999) were tested for amplification 2008). They are regarded as one of the "primitive" ant sub- and polymorphism in M. pavida. Only the primers de- families, having retained many ancestral characters, such signed for N. macrops were found to successfully ampli- as relatively small colonies and little queen-worker dimorph- fy homologous loci in
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