Parentage analysis

Make Him a Monogamy Junkie

The Monogamy Method

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The above characterization of mating systems was originally based on field and laboratory observations and experiments, and has been modified substantially in recent years. Key to our improved understanding of mating systems has been the application of molecular genetic data to parentage analyses, an approach that has allowed us to identify the genetic relationships of offspring and their putative parents. From these data it has become increasingly apparent that a social mating system can be very different from a genetic mating system. However, before we look at the findings that have come from parentage studies, we need to understand how we can determine whether or not a putative parent is in fact an offspring's genetic parent.

In studies of behavioural ecology we may wish to identify both of an offspring's genetic parents. In many cases we will be confident about the identity of the mother because in species that require parental care of young, she is unlikely to feed or care for offspring that she did not produce. Biological fathers, on the other hand, may be harder to identify because they may offer no parental care (most mammals) or may unknowingly care for young that are not their own (many birds). If we have genotypic data from an offspring and its putative parents then the simplest form of parentage analysis is exclusion. If an offspring's genotype at a single locus is AA then it must have received an A allele from each parent. If the mother's genotype is AB then we have no reason to believe that she is not a biological parent. If, however, the putative father's genotype is BC then we know that he cannot possibly be the genetic father of this chick. By using multiple loci we may be able to use this approach to exclude all males from the population except one, in which case we would conclude that the single non-excluded male is the genetic father.

If the number of candidate fathers in a population is small, and a sufficiently large number of polymorphic loci are used, then identifying the true father based on exclusions may be possible. It is often the case, however, that there are multiple males that we cannot exclude, in which case an alternative approach must be used to assign the true father. These assignments are often done using maximum likelihood calculations (Marshall et al., 1998). Likelihood ratios for each non-excluded male can be calculated by dividing the likelihood that he is the father by the likelihood that he is not the father. These likelihoods are based on both the expected degree of allele sharing between parents and offspring, and the frequencies of these alleles within the population. Likelihood ratios are calculated separately for each locus, and then the overall likelihood that a given male is the biological father is obtained by multiplying all likelihood values. This approach assumes that the loci behave independently from one another, i.e. they are in linkage equilibrium. The male with the highest likelihood ratio will generally be considered as the biological father, provided that his likelihood is sufficiently high.

Successful identification of parents depends in part on the molecular markers that are used. The likelihood of assigning the correct parent will often be directly proportional to the number and variability of the loci that are being genotyped, although there is also a risk that by using too many hypervariable markers we increase the chance of revealing a mutation that occurred between generations, in which case we may inappropriately exclude a biological parent (Ibarguchi et al., 2004). In general, the most useful markers for likelihood analysis in parentage assignments are microsatellites; dominant markers such as AFLPs also can be used, although many more loci are needed. In one study, researchers compared the performance of markers in assigning parentage within a stand of white oak trees (Quercus petraea, Q. robur) in northwestern France (Gerber et al., 2000). They found that fewer than ten microsatellite loci were sufficient for parentage studies, whereas 100--200 AFLP loci had to be used before parents could be assigned with comparable confidence. Of course, successful parentage analysis also depends on an adequate sampling regime. It is often not possible to sample every candidate parent from a population, particularly if dispersal is high, but the likelihood of finding the correct parent increases if a large proportion of breeding adults is included in the analysis.

Not surprisingly, assigning parentage is easiest when the identity of one parent is known, although it can also be done when neither parent is known. The authors of

Figure 6.1 Proportion of bottlenose dolphin offspring from which fathers could be excluded, and also to which fathers could be assigned, when the mothers were known and unknown. Data from Krutzen et a/. (2004)

a study of bottlenose dolphins ( Tursiops sp.) in Shark Bay, Australia, attempted to identify the fathers of 34 offspring with known mothers and 30 offspring for which neither parent was known. They tried initially to identify the fathers through exclusions and then, in the cases where multiple males remained unexcluded, they attempted to assign the correct father using likelihood ratios. In the group for which the mothers were known, exclusions allowed them to identify the fathers of 16 juveniles, and assignments subsequently identified a further 11 fathers at the 95 per cent confidence level. In the group for which neither parent was known, only five fathers could be identified through exclusions, and no further identification of fathers was made possible by assignments (Figure 6.1; Krutzen et al., 2004).

Extra-pair fertilizations

Parentage studies occasionally tell us that individuals are less promiscuous than was previously believed. Both male and female Arctic ground squirrels (Spermo-philus parryii plesius), for example, often copulate with multiple mates, but molecular genetic data have shown that more than 90 per cent of the pups whose mothers mated with more than one male were fathered by her first mate (Lacey, Wieczorek and Tucker, 1997; Figure 6.2). Far more common, however, is the finding that males and females are more promiscuous than their social mating systems would suggest. Extra-pair fertilizations (EPFs) occur when individuals choose mates that are not their social partners, a trend that has been documented in a wide range of taxa and in every type of mating system that involves pairbonds. Table 6.2 provides just a few examples of studies that have uncovered EPFs.

Figure 6.2 An Arctic ground squirrel (Spermophilus parryii plesius). Both males and females of this species typically mate with multiple partners and therefore, like the majority of mammals, its mating system is promiscuous. However, parentage studies have shown that most litters have only one genetic father (Lacey, Wieczorek and Tucker, 1997). This is therefore an unusual example of an animal whose genetic mating system is less promiscuous than its social mating system. Author's photograph

Figure 6.2 An Arctic ground squirrel (Spermophilus parryii plesius). Both males and females of this species typically mate with multiple partners and therefore, like the majority of mammals, its mating system is promiscuous. However, parentage studies have shown that most litters have only one genetic father (Lacey, Wieczorek and Tucker, 1997). This is therefore an unusual example of an animal whose genetic mating system is less promiscuous than its social mating system. Author's photograph

We can gain some idea of how pervasive this phenomenon is from the fact that fewer than 25 per cent of the socially monogamous bird species that had been studied up to 2002 were found to be genetically monogamous (Griffith, Owens and Thuman, 2002; see also Figure 6.3).

There are several evolutionary repercussions associated with EPFs. For one thing, their preponderance means that although it may be relatively easy to quantify a female's fitness based on the number of young that she produces, a male's fitness may be unrelated to the number of offspring that he rears. If there is a possibility that a male did not father all of the offspring produced by his mate then, in species that engage in biparental care, he is faced with a conundrum. Providing offspring and guarding them from predators is costly and is therefore worthwhile from an evolutionary perspective only if it increases a male's fitness. This clearly would not be the case if he were defending unrelated young. At the same time, males may risk losing all of their reproductive success if they neglect a brood that at least partially

Table 6.2 Some of the frequencies of extra-pair fertilizations (EPFs) that have been found in monogamous and polygamous species following molecular genetic parentage analyses. There are also species that very rarely engage in EPFs, and therefore the proportion of extra-pair young in all mating systems that involve pair-bonds ranges from essentially zero to more than half

Table 6.2 Some of the frequencies of extra-pair fertilizations (EPFs) that have been found in monogamous and polygamous species following molecular genetic parentage analyses. There are also species that very rarely engage in EPFs, and therefore the proportion of extra-pair young in all mating systems that involve pair-bonds ranges from essentially zero to more than half

Frequency

of extra-pair

Species

fertilizations

Reference

Social monogamy

Reed bunting (Emberiza schoeniclus)

55% of young

Dixon etal. (1994)

Common swift (Apus apus)

4.5% of young

Martins, Blakey and

Wright (2002)

Australian lizard (Egernia stokesii)

11% of young

Gardner, Bull and

Cooper (2002)

Island fox (Urocyon littoralis)

25% of young

Roemer et al. (2001)

Hammerhead shark (Sphyrna tiburo)

18.2% of litters

Chapman et al. (2004)

Social polygyny

Gunnison's prairie dog

61% of young

Travis, Slobodchikoff

(Cynomys gunnisoni)

and Keim (1995)

Dusky warbler (Phylloscopus fuscatus)

45% of young

Forstmeier (2003)

Rock sparrow (Petronia petronia)

50.5% of young

Pilastro et al. (2002)

Social polyandry

Wattled jacana (Jacana jacana)

29% of young

Emlen, Wrege and

Webster (1998)

Red phalarope (Phalaropus fulicarius)

6.5% of young

Dale et al. (1999)

comprises their genetic offspring, and therefore paternal care often appears to be unconditional. In some cases, however, males appear to hedge their bets and provide parental care in proportion to their confidence in paternity. This was the strategy followed by males in a population of socially monogamous reed buntings (Emberiza schoeniclus) that raise two broods each year. A comparison of EPF

0 5 10 15 20 25 30 35 40 45 50 55 Proportion of EPFs (%)

Figure 6.3 Proportion of EPF offspring within the broods of 95 socially monogamous or polygynous bird species. Adapted from Griffith, Owens and Thuman (2002) and references therein frequencies, along with observational data, showed that of the two broods, the males provided most food to the one in which they had the highest confidence of paternity (Dixon et al., 1994). Similar adjustments of male parental care in response to levels of genetic paternity have been found in a number of other taxonomic groups including bluegill sunfish (Lepomis macrochirus; Neff, 2003) and dung beetles (Onthophagus Taurus; Hunt and Simmons, 2002).

Another important consequence of EPFs is that, even in socially monogamous species, males do not have to form pair-bonds in order to achieve reproductive success. Genetic data have revealed successful fertilizations by floater (also known as sneaker) males, i.e. males who are not pair-bonded. Tree swallows (Tachycineta bicolor; Figure 6.4) typically engage in a high frequency of EPFs (around 55 per cent Conrad et al., 2001), and in one study at least 8 per cent of these were accomplished by unmated males (Kempenaers et al., 2001).

The potential reproductive success of unmated males has been further demonstrated by species that embrace a variety of reproductive strategies, such as the bluegill sunfish (Lepomis macrochirus). In bluegill populations in eastern Canada, parental males mature when they are around 7 years old, at which time they construct nests and attract females. They then defend the nest site, eggs and hatchlings against any intruders until the young are old enough to leave the nest. Sneaker males, on the other hand, may be only 2 years old and they attempt to

Figure 6.4 A female tree swallow (Tachycineta bicolor) tending to her nest at the Queen's University Biological Station in Ontario, Canada. Researchers have been studying tree swallows here since 1975. Photograph provided by P.G. Bentz and reproduced with permission

fertilize eggs by darting into a nest and quickly releasing sperm while the resident male is spawning with a female, in the hope that they too will fertilize some of the eggs. A third strategy is followed by satellite males, which are usually aged 4-5 years and use colour and behaviour to mimic females. This disguise sometimes enables them to deposit sperm in the nest while the unsuspecting resident male is busy with a spawning female. Molecular studies have shown that the parental males achieve an average of 79 per cent of fertilizations, with the remaining 21 percent achieved by sneaker or satellite males. Because about 80 per cent of the males in the studied population were parental males, the overall fitness of each of the three male strategies may be similar, although estimates of lifetime reproductive success are needed before this suggestion can be confirmed (Philipp and Gross, 1994; Neff, 2001; Avise et al, 2002).

When weighing the fitness costs and benefits that are associated with alternative reproductive tactics we must also consider the degree to which males are cuckolded. Different rates of EPFs have been found in species that engage in both monogamy and polygyny. Comparisons of EPFs in willow ptarmigan (Lagopus lagopus; Figure 6.5) and house wrens (Troglodytes aedon), for example, have shown that the benefits to males of attracting multiple mates are often counteracted by an increased level of cuckoldry in polygynous males compared with monogamous males (Freeland et al., 1995; Poirier, Whittinghan and Dunn,

Figure 6.5 A male willow ptarmigan (Lagopus lagopus) in the sub-Arctic tundra of northwest Canada defends his territory at the start of the breeding season. Author's photograph

2004). In other words, although polygynous males appear to have a greater number of offspring, an increased frequency of EPFs in their broods means that they may not have fathered any more chicks than the monogamous males. If there is no increase in fitness associated with the additional costs that are incurred by polygynous males, who must guard relatively large territories, multiple mates and numerous offspring, then social monogamy should prevail.

6.1 Conspecific brood parasitism

Although extra-pair fertilizations provide the main explanation for the differences that we often find between genetic and social mating systems, genetic evidence has shown that in some bird populations a resident female may not be the biological mother of the young that are in her nest. This is because of a behaviour known as conspecific brood parasitism (CBP), which occurs when females lay their eggs in the nests of other conspecific birds. In species that require biparental care, the reproductive success of both the resident male and the resident female will suffer because they will end up rearing a bird that is not their own (Rothstein, 1990); the parasitic female, on the other hand, will benefit from an increase in fitness. A related behaviour known as quasi-parasitism (QP) occurs when a parasitic female lays her egg in the nest of the biological father with whom she achieved the EPF. In this case, it is only the resident female whose fitness is likely to suffer, because she will be the only one rearing an unrelated chick. Although much less common than EPFs, brood parasitism has been documented at low frequencies in a number of socially monogamous bird species, including European starlings (Sturnus vulgaris; Sandell and Diemer, 1999) and white-throated sparrows (Zono-trichia albicollis; Tuttle, 2003).

Conspecific brood parasitism also occurs in some socially monogamous fish species, such as the largemouth bass (Micropterus salmoides) that engages in biparental care for up to a month after eggs hatch. In one study, genetic monogamy was the norm in this species, although in 4/26 offspring cohorts there was evidence that some of the eggs had been deposited by an extra-pair female (DeWoody et al., 2000). Parentage studies have also revealed brood parasitism in polygamous species, such as the polygynandrous Australian magpie (Gymnorhina tibicen) that lives in groups that strongly defend their territories from outsiders. Despite this territorial nature, one study found that an astounding 82 per cent of young had been fathered by males from outside the group and that 10 per cent of young were the result of CBP by females from outside the territory (Hughes et al., 2003).

Figure 6.6 A blue-footed booby (Sula nebouxii) on Isla San Cristobal in the Galápagos Archipelago. This is a socially monogamous bird that engages in relatively high levels of extra-pair fertilizations. The colourful feet are used in courtship displays, and males prefer females with particularly bright feet (Torres and Velando, 2005). Author's photograph

Figure 6.6 A blue-footed booby (Sula nebouxii) on Isla San Cristobal in the Galápagos Archipelago. This is a socially monogamous bird that engages in relatively high levels of extra-pair fertilizations. The colourful feet are used in courtship displays, and males prefer females with particularly bright feet (Torres and Velando, 2005). Author's photograph

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