360 New Zealand Journal of Ecology, Vol. 34, No. 3, 2010
SHORT COMMUNICATION
Multiple paternity in wild populations of invasive Rattus species
Steven D. Miller
*
, James C. Russell, Hamish E. MacInnes, Jawad Abdelkrim and Rachel M. Fewster
Department of Statistics, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand
*Author for correspondence (Email: smiller@stats.waikato.ac.nz)
Published on-line: 21 April 2010
Abstract: Multiple paternity within litters has been recorded among a variety of small mammal species, including some
species of rodents. Although multiple mating has been observed in wild Rattus populations, whether such mating results
in litters with multiple paternities has not been established previously. For studies involving invasive species, it is useful
to be aware of the level of genetic diversity a single pregnant invader can bring to a population. Multiple paternity is a
means of providing additional genetic diversity to founding populations of rats on islands, which might improve population
itness. We used a genetic approach to conirm that multiple paternity occurs in wild populations of two rat species (Rattus
norvegicus and R. rattus) in New Zealand. This was accomplished by genotyping litters of embryos in pregnant females,
and subtracting the known maternal alleles to ind the number of paternal alleles necessary to form the litter. The number
of paternal contributors cannot be overestimated by this method, beitting a conservative approach to the detection of
multiple paternity, but can be underestimated. We used simulations to investigate the level of underestimation likely under
two possible scenarios involving multiple paternity.
Keywords: founder; genetics; microsatellite; Rattus norvegicus; Rattus rattus
Introduction
Rattus norvegicus (Norway rats) and R. rattus (ship rats) are two of
the three species of Rattus classiied as invasive (Howald et al. 2007).
Following their introduction to New Zealand by Europeans, both
species have had a devastating impact on native species (Bell 1978;
Atkinson 1985; Towns et al. 2006). The establishment and maintenance
of pest-free island sanctuaries are important conservation goals, so
investigation of island invasion processes by rats is of particular
interest for conservation in New Zealand (Russell et al. 2008b).
Island populations founded by a small number of invaders are
vulnerable to the adverse effects of low genetic diversity. Low genetic
diversity reduces the survival of individuals, through inbreeding
depression, and limits the ability of the population to resist disease
and adapt to environmental conditions (Jamieson 2009; Russell
et al. 2009a). If pregnant females are capable of carrying offspring
with multiple fathers, a single pregnant invader might be carrying
the genes of three or more founders. Such multiple paternity would
act against inbreeding depression and increase the chance of the
population establishing and surviving in the long term.
Population establishment by pregnant females is considered a
serious threat for many island sanctuaries. In northern New Zealand,
female rats are capable of pregnancy throughout the year (Innes 2001;
Innes et al. 2001). It is not known whether wild rats avoid mating
with siblings or parents; however, for some species of rodents there
is evidence that even small kinship differences can affect mating
behaviour (Ryan & Lacy 2003). Multiple paternity would decrease
relatedness within a litter, and might therefore lead to more breeding
between litter-mates as well as better survival of their offspring. It is
potentially a signiicant factor in enabling rat populations to establish
from a very small number of invaders, perhaps just one pregnant
female. The purpose of this study was to determine whether multiple
paternity occurs in wild populations of R. norvegicus and R. rattus
in New Zealand.
The mating behaviour of R. norvegicus varies according to
population density. At low densities, males hold territories and guard
groups of females for exclusive mating (Calhoun 1963; Waterman
2007). At high densities, the social structure shifts to a despotic
system where territories are ill-deined and males rank themselves
in dominance, generally according to age (Barnett 1958; Lott 1984;
Waterman 2007). In this situation, males are unable to defend females
for exclusive mating, and roving bands of males will attempt to mate
with any female that comes into oestrus, resulting in multiple mating
(Calhoun 1963; Robitaille & Bovet 1976). Although multiple mating
raises the possibility of multiple paternity, it does not necessarily lead
to multiple paternity. It might be that only the ittest male’s sperm is
selected to fertilise the female’s eggs.
The mating behaviour of R. rattus has received less attention
than that of R. norvegicus. Ewer (1971) and Corbet and Southern
(1977) describe similar density-dependent behaviour to R. norvegicus
among R. rattus populations that were commensal with humans.
However, Hooker and Innes (1995) found that wild R. rattus in
New Zealand that were non-commensal with humans tended to prefer
solitude. Males did not maintain groups of females in their territories,
even when population density was low. In this social arrangement,
it is more dificult for a male to ensure he mates exclusively with
particular females.
Multiple paternity has not previously been established at the
genetic level for wild populations of R. norvegicus or R. rattus.
Heiberg et al. (2006) inferred multiple paternity in R. norvegicus
removed from the wild, but they did not use known maternal genotypes.
Instead, parents were assigned probabilistically by choosing the
male–female pair that most likely contributed their alleles to a juvenile
rat. The natural breeding behaviour of the rats might also have been
affected by being kept under experimental conditions. In this study,
we genotyped litters of embryos inside pregnant females, together
with the corresponding maternal tissue, to determine the number of
paternal alleles required to form the litter. This approach will conirm
the occurrence of multiple paternity if there is some genetic locus at
which more than two paternal alleles are required.
Methods
Sampling
Rattus norvegicus were trapped on the island of Pakihi (114 ha) in
the Hauraki Gulf, Auckland, New Zealand, as part of a related study.
Thirty Tomahawk live-traps and 20 Victor snap-traps baited with
chocolate paste were deployed over the summers of 2004 to 2006,
returning 49 rats (Russell et al. 2008a). Three visibly pregnant female
New Zealand Journal of Ecology (2010) 34(3): 360-363 © New Zealand Ecological Society.
Available on-line at: http://www.newzealandecology.org/nzje/