Can incest within cooperative breeding groups be detected using DNA fingerprinting?

Abstract

Although generally considered a rare phenomenon, in-cest has been observed in a number of populations ofbirds and mammals in which dispersal is limited (Green-wood et al. 1978; Bulger and Hamilton 1988; Gibbs andGrant 1989; Packer and Pusey 1993; Keller and Arcese1998). In cooperatively breeding animals where off-spring remain in their natal territory as adults, the oppor-tunity for incest may be substantial (Ligon and Ligon1990). Inbreeding avoidance mechanisms ensure thatcases of incest in the cooperatively breeding acornwoodpecker (Melanerpes formicivorus) are exceedinglyrare, and groups whose membership consists of onlyclosely related members of the opposite sex may foregobreeding for up to 3 years if membership remains unal-tered (Koenig et al. 1998). Incest is avoided in the su-perb fairy wrenMalurus cyaneusthrough a differentmechanism: although offspring remain on their natal ter-ritory, females seek extra-group matings, particularlywhen many sons remain as helpers in the group (Brookeret al. 1990; Mulder et al. 1994). Few other studies of co-operatively breeding populations have verified genetical-ly whether or not incest occurs.To date, most studies that have looked at genetic rela-tionships within groups of cooperatively breeding ani-mals have used multilocus DNA fingerprinting (Rabenoldet al. 1990; Jones et al. 1991; Packer et al. 1991; Bruce etal. 1996; Whittingham et al. 1997; Lundy et al. 1998). Inseveral cases, the authors appear not to have appreciatedthat this technique does not allow the detection of parent-offspring incest. While some have acknowledged the lim-itations of the data and were careful not to make inferenc-es beyond the scope of the technique (Haig et al. 1994;Dickinson et al. 1995; McRae 1996; Koenig et al. 1998),others have simply ignored the possibility of incest. Sincegenetic data of this nature are often compiled to drawgeneral conclusions about levels of reproductive skew(Reeve and Keller 1995), and inbreeding (Heinsohn et al.1990; Pusey and Wolf 1996), it is important that this pos-sibility is not overlooked. We outline here why conven-tional DNA fingerprinting is limited, and in some casesunsuitable, for studying parentage in social animals, anddiscuss the power of typing with microsatellite markers.The technique of multilocus DNA fingerprinting suf-fers from the constraint that individual bands cannot beassigned to known loci making it impossible to deter-mine whether a given band is of paternal or maternal ori-gin (Jones et al. 1991; McRae 1996; Danforth andFreeman-Gallant 1996). Careful analyses are required todetermine whether or not bands are segregating indepen-dently. For example, bands may be consistently scoredtogether (linkage), or they may appear mutually exclu-sive (allelism). Although segregation analyses can beused to calculate the probability of error due to non-inde-pendence, this is not always helpful for parentage analy-sis when parental candidates are the first-order relativesof other parental candidates.Paternity analysis with multilocus DNA fingerprintsrelies on the existence of ‘diagnostic’ bands to excludeindividuals from parentage. The problem with analyzingfingerprints of cooperative groups arises uniquely whenthere is an adult helper in the group that is the full off-spring of the dominant pair. This is a very commongroup structure among avian cooperative breeders re-ferred to as ‘simple’ family groups (Emlen 1995). Takethe example of a dominant pair whose adult son remainsin the group as a helper. When a chick is the offspring ofthe dominant male and female (i.e., the full sibling of thehelper), assuming the identity of the mother is reliable,there will often be (paternal) bands found in the finger-prints of the chick and the dominant male that are notfound in that of the helper son. Thus it is usually possi-ble to exclude the son from paternity. However, if achick is the product of mother-son incest, it is impossibleto exclude the dominant male (i.e., the actual grandfather