Behavioral Ecology Vol. 14 No. 4: 481-485
© 2003 International Society for Behavioral Ecology
Do male golden egg bugs carry eggs they have fertilized? A microsatellite analysis
a Department of Biology, University of Oulu, Box 3000, FIN-90014 Oulu, Finland b Department of Zoology, Stockholm University, S-10691 Stockholm, Sweden
Address correspondence to W.T. Tay, who is now at the Department of Genomics and Bioinformatics, Roslin Institute, Roslin, Midlothian EH25 9PS, UK. E-mail: weetek.tay{at}bbsrc.ac.uk.
Received 20 July 2001; revised 12 April 2002; accepted 28 August 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In the golden egg bug, Phyllomorpha laciniata (Heteroptera, Coreidae), both males and females carry eggs on their back. Although females cannot carry their own eggs, males may carry eggs that they have fertilized. If males carry eggs they have fertilized, their behavior may be interpreted as paternal care. In this article, we provide genetic data for paternity assignment of eggs carried by 40 males collected from the field. The males and the eggs were typed by using four highly polymorphic microsatellite DNA markers. Out of the 247 eggs typed, 87% were excluded from the father-offspring relationship based on single-locus (least conservative exclusion) mismatches. Under the more conservative (exclusion by at least two single locus mismatches) method, 78% of the eggs were nonpaternal. Relatedness estimates further supported our paternity analyses. The average relatedness of the eggs to the carrying males was low (bem = -0.052 ± 0.024 SE). Within the population, males were unrelated to each other (bmm = -0.004 ± 0.0002 SE), as were the eggs carried by individual males (beggs = -0.004 ± 0.0001 SE). This first genetic study on the breeding system of the golden egg bugs did not find any support for the claim that egg carrying functioned as paternal care, nor did it support kin selection as explanation for conspecific egg carrying.
Key words: microsatellite, paternity, Phyllomorpha laciniata, relatedness.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Most insects face high offspring mortality because eggs are left undefended. In some species, females may increase the probability of offspring survival by placing their eggs in concealed locations, by constructing nests, by modifying the environment, or by defending eggs (Eickwort, 1981
; Janz, 2002; Tallamy, 1984; Tallamy and Wood, 1986). In the overwhelming majority of insect species, eggs are not defended. However, if egg defense occurs, it is commonly performed by females (Tallamy, 1984, 1994), and only rarely are males involved in care taking (Ridley, 1978; Smith, 1997). Male reproductive success is often limited by the number of successful matings rather than by the number of gametes produced (Trivers, 1972). Paternal care is therefore not expected if time allocated to current offspring results in lost mating opportunities. Furthermore, males are not expected to care for the offspring if the probability of paternity is low (Grafen and Sibly, 1978; Maynard Smith, 1977; Ridley, 1978; Scott, 1990; Trivers, 1972; Werren et al., 1980; Zeh and Smith, 1985). In insects, females possess the ability to store sperm, and sperm competition is common (Parker, 1970). This, together with the occurrence of multiple mating in females, can lead to uncertainty of paternity and increases males' risk of being cuckolded.
In the golden egg bug, Phyllomorpha laciniata, females lay eggs on the backs of both male and female conspecifics. In many populations, arthropod eggs cannot survive unless carried by living conspecifics owing to ant predation (Du Merle et al., 1978; Kaitala, 1996; Retana et al., 1991). A plausible evolutionary explanation for the peculiar oviposition behavior is that by using conspecifics as oviposition sites, females increase their offspring survival. However, finding an evolutionary explanation for why conspecifics carry eggs is more problematic, especially if the costs of carrying eggs are high. So far, there is no evidence for egg carrying being beneficial to the carrier. On the contrary, egg carrying has been shown to attract predators (Kaitala and Axén, 2000; Kaitala et al., 2000; Reguera and Gomendio, 1999). Generally, individuals are not expected to help each other if helping is costly, although costly acts may be performed if the receiver is a relative (Connor, 1995; Hamilton, 1964; Trivers, 1971). In the case of the golden egg bug, a likely explanation for the egg-carrying behavior could therefore be that individuals are carrying their offspring. Although females do not carry their own eggs because they are unable to oviposit on their own backs, males may carry eggs they have fertilized. The golden egg bug is a highly polyandrous species, and females may mate with different males before laying a clutch, which means that paternity assurance is expected to be important. In the laboratory, copulation time is long, often lasting more than 20 h (Kaitala and Miettinen, 1997), and this may indicate that males try to ensure their paternity. Under natural conditions, however, it is not known how often males carry eggs they have fertilized: a situation that would require that there is last male sperm precedence and that females, once copulation is terminated, quickly deposit some eggs on the backs of their mating partner.
Molecular genetic techniques such as microsatellite DNA markers have been applied successfully in studying paternity (see DeWoody et al., 1998; Foitzik and Heinze 1998; Rossiter et al., 2000; Questiau et al., 1999; Taylor et al., 2000; for a review, see Hughes, 1998). The use of microsatellite DNA markers therefore offers great potential to decipher the parentage of eggs carried by male golden egg bugs and, hence, a way forward to understanding the nature of the egg-carrying behavior. In this article, we use microsatellite DNA markers to investigate how often males carry eggs that they have fertilized, and to study the likelihood that the eggs are laid by close relatives.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study site and background
We collected males carrying eggs from their natural habitat close to El Puerto de Santa Maria, Andalusia, southern Spain, in late April 2000 (Katvala and Kaitala, 2001
). Samples were placed in 96% ethanol and stored at -20°C within 24 h after collection. Individual males were subsequently transferred into separate Eppendorf tubes containing fresh 96% ethanol. Only eggs that remained firmly attached to the back of individual males were used for paternity analyses. Eggs were removed from the male's back by using sterile forceps and were placed individually into separate tubes for DNA extraction.
DNA extraction and polymerase chain reaction protocols
A partial P. laciniata DNA library was constructed following the method of Thorén et al. (1995) with slight modifications. The library was screened with (CT)10, (GT)10, and (ATT)10 oligonucleotide probe end-labeled with DIG detection (DIG [Digoxigenin] Luminescent Detection Kit, Boeringer-Mannheim). Positive recombinant clones were sequenced, from which microsatellite DNA primers were designed by using the program OLIGO. DNA from individual males (single legs crushed in liquid nitrogen) and eggs were extracted in separate Eppendorf tubes by using 5% Chelex® in a final volume of 100 µL following the methods of Tay and Crozier (2000). Genotypes of the males and the eggs were typed by using four microsatellite markers: Plac 47, Plac 109, Plac 38, and Plac 95B. Polymerase chain reaction (PCR) amplification was performed in 10 µL final volume consisting of 0.16 mM each dNTP, 10 mM Tris–HCl at pH 8.8, 50 mM KCl, and 0.1% Triton X-100; specific MgCl2 concentration (Table 1); 0.6 µM of fluorescent-labeled primers and equal concentration of unlabeled complementary primer; 0.4 U of DyNAzymeTM DNA polymerase (Finnzymes); and 2.5 µL of template DNA. The PCR profile consisted of a 2.5-min initial denaturation step at 95°C, followed by 35 cycles of 30 s at 95°C, 90 s at 50°C, and 7 s at 70°C. PCR products were separated by electrophoresis on ABI 377 automated sequencer (PerkinElmer).
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Microsatellite DNA genotypes were scored by using the program Genotyper® 2.0 (ABI Prism). Allelic mismatches between the males and the eggs were checked visually, and reamplification of samples was performed if necessary. To minimize the risk of false parentage exclusion (Schlotterer and Pemberton, 1994
), we excluded eggs that failed to amplify at three out of the four loci.
Paternity analyses
Microsatellite DNA markers can be affected by null (nonamplifying) alleles; thus, false parentage exclusion may occur when these markers are used in parentage studies (Jones et al., 1998; Pemberton et al., 1995; Primmer et al., 1995). When a marker is affected by null alleles, a heterozygote individual will be scored as a homozygote if one of the two alleles is unsuccessfully amplified. Similarly, an individual will have no allelic product at the locus when carrying a homozygous null allele. In the present study, null homozygotes and failed PCR amplifications (e.g., owing to poor DNA quality) are treated as missing data. To estimate the frequencies of null alleles for our markers, the method presented by Brookfield (1996) was used. To determine the parentage exclusionary power of our microsatellite markers, assuming both parents were unknown, we followed the methods of Jamieson (1994).
Because of the possible presence of null alleles, two exclusion methods were used: the least conservative exclusion method (I) and the more conservative exclusion method (II). Under method I, exclusions by single-locus mismatches were considered valid if microsatellite genotypes for the loci fulfilled at least one of the following three criteria: (1) both male and offspring were heterozygous and shared no alleles (i.e., genotypes of the male = AB; genotypes of the egg = CD); (2) the male was heterozygous, and the egg was scored as homozygous for an allele not present in the male (i.e., male = AB; egg = DD); or (3) the egg was heterozygous, whereas the male was scored as homozygous for an allele not present in the egg (i.e., male = AA; egg = CD). If the egg and the male were both homozygous for different allele (i.e., male = AA; egg = CC), exclusion of paternity was not possible because they both could share a same null allele.
Under the more conservative exclusion method (II), all homozygotes were treated as partial genotypes (i.e., as partial single known genotypes and therefore compatible with all other genotypes), and exclusions were verified by using at least two loci. Exclusion by single-locus mismatch was therefore only possible if the male and the egg were both heterozygous and shared no alleles at the locus. Further, to minimize the probability of false exclusion owing to genotype scoring errors, if either the male or the egg was a nonidentical homozygote for the loci, an additional single-locus mismatch was required to establish a non–father-offspring relationship (i.e., at least two single-locus mismatches were required).
Relatedness analysis
We used the program Relatedness 5.0.6 (Goodnight, 1994; Queller and Goodnight, 1989) to estimate average relatedness between the males (bmm), between eggs carried by individual males (beggs), and between the males and their eggs (bem). Relatedness estimates were calculated based on the population allele frequencies. SEs were obtained by jackknife over loci. Average relatedness values were tested against the hypothesis of nonrelatedness (b = 0) using one-tailed t tests, with three degrees of freedom.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Marker characteristic and PCR amplification rate
Assuming that both parents were unknown, the parentage exclusion probability for microsatellite loci Plac 47, Plac 109, Plac 38, anzd Plac95B were 0.849, 0.528, 0.665, and 0.888, respectively (average exclusionary power = 0.733). The mean expected heterozygosity for the four loci was 0.917, with a mean of 47.3 alleles detected per locus. High frequencies of null alleles (r) were estimated for all loci, with frequencies ranging from 0.108 to 0.242 (Table 1). The DNA sequences of microsatellite markers, GenBank accession numbers, Mg2+ concentrations, range of allele frequencies, and the expected and observed heterozygosity for the four loci are provided in Table 1.
All males amplified successfully for all loci, with the exception of male 36 that failed to amplify at locus Plac 38. Amplification of eggs generally gave good PCR products, although 23, 35, one, and five eggs failed to amplify at loci Plac 38, Plac 47, Plac 95B, and Plac 109, respectively. Two eggs were excluded from the parentage exclusion analysis owing to poor overall PCR amplification (M34-egg 5, PCR failed at three loci; M40-egg 5, PCR failed at all loci). Overall, 247 eggs were typed for this study.
Paternity analysis
The least conservative exclusion method (I) excluded the father-offspring relationship from a male-egg pair, if alleles of a single locus fulfilled one of the three criteria specified: (1) both the male and the egg were heterozygous and shared no alleles; (2) the male was heterozygous, and the egg was scored as homozygous for an allele not present in male; or (3) the egg was heterozygous, and the male was scored as homozygous for an allele not present in the egg. Based on the least conservative method, 87% of eggs (215 of 247) were excluded and thus were not carried by the father. Although paternal exclusion requires only one out of the three criteria to be fulfilled, most of the eggs had nonidentical genotypes with the male at two, three, or four of the loci. Thus, 15% of eggs were single-locus exclusions, and 32% had nonidentical genotypes with the male at two loci, 29% at three loci, and 11% at all four loci.
Under the more conservative exclusion method (II), a single-locus exclusion was accepted only if both male and the egg were heterozygous and shared no alleles at the locus, otherwise at least two single-locus mismatches were required for exclusion. According to this method, 78% of eggs (192 of 247) were excluded from the father-offspring relationship; of which 6% of the eggs were excluded based on the presence of nonidentical heterozygous alleles in one of the four loci examined, whereas 72% of the eggs were excluded by using at least two loci. Table 2 summarizes the number of eggs excluded from each of the 40 males according the two exclusion methods.
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Only five eggs, carried by two males, shared alleles over all four loci with the carrying male. No exclusion was possible for 11% (n = 27) of the eggs because these eggs and the male egg-carriers were homozygous and thus potential null heterozygotes.
Relatedness analyses
Relatedness estimates of the males and eggs based on microsatellite DNA data indicated that within the population, males were unrelated to each other (bmm = -0.004 ± 0.0002 SE). In addition, eggs carried by individual males were also unrelated to each other (beggs = -0.004 ± 0.0001 SE), indicating that these eggs have been oviposited by several unrelated females. The average relatedness of eggs carried by the males was low (bem = 0.052 ± 0.024 SE; t = 2.167, p = ns), which further supports the results from our paternity analysis.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The most likely evolutionary explanation for the peculiar egg carrying behavior would be that individuals carry their own offspring. The egg carrying behavior of male golden egg bugs has also been regarded as a form of paternal care (Reguera and Gomendio, 1999
; Ridley, 1978; Wilson, 1971; but see Kaitala, 1996; Kaitala and Miettinen, 1997; Kaitala et al., 2001; Miettinen, 2001; Miettinen and Kaitala, 2000; Tallamy, 1994). However, if the primary function of egg carrying is paternal care, then it would be expected that: (1) only males carry eggs, and (2) males only carry eggs that they have fertilized. Contrary to this expectation, one-third of the eggs are carried by females (Reguera and Gomendio, 1999; Kaitala,1996; Kaitala and Miettinen, 1997). Further, laboratory experiments have shown that males, while courting, commonly received eggs from females they have not mated with (Kaitala, 1998; Kaitala and Miettinen, 1997; Miettinen and Kaitala, 2000). Using highly polymorphic microsatellite DNA markers, we have shown that male golden egg bugs commonly carried eggs that they had not fertilized. Based on the least conservative exclusion method (I), 87% of eggs in this study could be excluded from being offspring to the carrying male. Under the more conservative exclusion method (II), 78% of eggs were identified as not being the offspring of the males that carried them. Thus, available data to date do not provide support for the claim that egg carrying has evolved, or is maintained, as a paternal care strategy.
Laying eggs on the backs of other conspecifics is an effective strategy of decreasing egg mortality (Kaitala, 1996). Female bugs therefore use all opportunities to oviposit on the backs of conspecifics, regardless of sex and mating history (Kaitala and Miettinen, 1997; Kaitala, 1998; 1999; Miettinen, 2001; Miettinen and Kaitala, 2000). Previous experiments showed that carrying eggs increased the risk of predation (Reguera and Gomendio, 1999; Kaitala and Axén, 2000; Kaitala et al., 2000), and bugs sometimes actively scrape eggs from their own backs, indicating that egg carrying is costly (Kaitala, 1996, 1999). However, receiving eggs is often unavoidable for the bugs. For example, while mating, a pair cannot resist oviposition attempts by other females except by terminating copulation (Kaitala and Miettinen, 1997). Females also commonly lay eggs on courting males (Kaitala, 1998; Miettinen and Kaitala, 2000). Although some oviposition attempts are resisted, in the laboratory when reared in small enclosures, bugs commonly show no resistance against receiving eggs (Kaitala, 1998; Kaitala and Miettinen, 1997; Miettinen and Kaitala, 2000). Although bugs in the laboratory cannot escape or hide egg-laying females, it is unclear whether bugs can resist oviposition attempts under natural circumstances. Whether receiving an egg is preceded by resistance or not, ovipositing females are behaving like intraspecific parasites because other individuals are made to carry their eggs.
The golden egg bug is a highly polyandrous species, and females may mate with different males before laying a clutch. Although the long duration of copulation (more than 20 h under laboratory conditions) could be viewed as a paternity assurance mechanism, eggs are rarely laid directly after copulation, as copulation and oviposition is often separated by more than a day (Kaitala and Miettinen, 1997). This delay between copulation and oviposition is expected to decrease male paternity certainty if the female copulates with another male before oviposition (Parker, 1970), although "mate guarding" can minimize this risk. Sexual competition has also been shown to affect male eagerness to carry egg in the golden egg bug. Males were more eager to carry their own eggs when sex ratio was male-biased (Miettinen and Kaitala, 2000).
Although we have analyzed only males and their eggs, our genetic data may be applied further. Relatedness analyses indicated that apart from the fact that males were carrying eggs they had not fertilized, the males were also unrelated to each other, as were the eggs within an egg batch. Thus, genetic data indicated that males generally carried eggs of diverse maternal and paternal origins. The breeding system of the golden egg bugs leads to complicated social interactions among individuals, resulting in unusual conflict of interest between the sexes. Courting puts males at risks of receiving costly eggs because females may exploit males' sexual interest by laying eggs on them. Females' need to find safe oviposition sites to secure the survival of their offspring is further evident in their nondiscriminatory egg-dumping behavior on both male and female conspecifics. Available data to date therefore lend support to the system being driven by egg-laying females behaving like intraspecific parasites (Kaitala, 1998, 1999; Kaitala and Miettinen, 1997; Miettinen, 2001).
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ACKNOWLEDGEMENTS |
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We are grateful to Susanne Gustafsson and Peter Thorén for their valuable help at the early stage of the laboratory work. We thank Auli Karhu for help with laboratory techniques and Hannele Parkkinen for running microsatellite gels. Mari Katvala, Hanna Suutari, and Juan A. Amat helped with the sample collection. Mari Katvala and Craig Primmer provided helpful discussion on various aspects of this project. We also thank the two anonymous referees for their valuable comments. This work was support by grants from the Finnish Academy (project no. 42587) to A.K and W.T.T.
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