Introduction
Mating patterns are important because they determine which alleles unite
in the same individuals to be tested by selection. When individuals with
particular combinations of genotypes are more or less likely to mate
with each other than expected by chance, this can bring together
combinations of beneficial alleles in the offspring. It can also bring
recessive deleterious alleles together and cause inbreeding depression.
There may also be variation between individuals in how many mates, and
hence offspring, they have, causing heritable changes in the population.
We would like to understand who mates with whom, and characterise
variation in reproductive success.
For many plants mating is mediated by animal pollinators. Two aspects of
pollinator behaviour are important. Firstly, pollinators make decisions
about which plants to visit based on the phenotypes of the plants. They
may preferentially visit flowers that are especially attractive or
rewarding, causing differences in reproductive success between plants.
There is an extensive literature exploring differences in the female
component of reproductive success measured through seed set. However,
although the majority of flowering plants are hermaphrodites [ref?],
the male component of fitness, reflected in successful pollen export to
other plants, has received much less attention, because this requires
accurate assignment of paternity in seeds. Since every offspring
receives exact half its genetic material from the mother and half from
the father, by neglecting variation in male fitness we also potentially
miss substantial variation in overall reproductive success.
Secondly, it is more energy efficient for pollinators to transition
between plants that are close to one another than to move at random
between plants. This means that plants are more likely to mate with
close neighbours than more distant plants. The distribution of pollen
dispersal distances is described by the pollen dispersal kernel. In
plants, it is common to find that the dispersal kernels that show strong
leptokurtosis, or overdispersion; most dispersal is between close
neighbours, but there is a ’fat tail’ of long-distance dispersal events
that cause the dispersal kernel to decay more slowly than exponentially.
Although these events are relatively rare, they contribute
disproportionally to the spread of migrants, allowing populations to
expand rapidly in space, and to homogenise distant populations. This is
especially important in a hybrid zone, where divergent populations meet
and exchange migrants. Here, the extent to which alleles at individual
loci are able to introgress across the hybrid zone is determined by the
balance between the homogenising effect of dispersal, and selection
against migrant alleles keeping populations spatially distinct. Given
estimates of dispersal distance and distribution of alleles in space we
can infer the strength of selection acting on those alleles. Accurate
estimates of the shape of the dispersal kernel are this invaluable in
understanding the evolutionary processes acting in natural populations.
Pedigree reconstruction has emerged as a powerful tool to investigate
both both differences in mating success and dispersal \cite{Pemberton2008}.
The idea is to reconstruct mating events by identifying the parents of a
set of offspring asssuming Mendelian inheritance based on shared alleles
at loci for which offspring and candidate parents have been genotyped.
This is most successful when as much informative data as possible can be
included in the analysis \cite{Wang2007}. One way to achieve this is to
jointly infer sibling relationships and the paternity of those sibships
. Likewise, inference of parentage jointly with other biological
parameters that influence mating, such as those related to dispersal or
mating success increases the accuracy to infer both the pedigree and
biological parameters \cite{Hadfield2006,Neff2001}. It follows from this that an even more powerful
approach would be to unify these approaches and jointly infer parentage,
sibships and biological parameters. However, we currently lack software
which is able to do this efficiently for modern SNP data.
Here, we examine a hybrid zone between two subspecies of the snapdragon, Antirrhinum majus that differ for flower colour. Flower colour in A. majus is controlled primarily by the genes Rosea ,
controlling the distribution of magenta anthocyanin pigments, and Sulfurea , controlling the distribution of yellow aurone pigments.
In the Vall de Ribès in the Spanish Pyrenees, the yellow-flowered A. m. striatum and the magenta-flowered A. m. pseudomajus meet and form a narrow hybrid zone where loci at Rosea and Sulfurea recombine to give rise to six flower-colour morphs.
Alleles at these loci nevertheless form sharp clines consistent with
selection against recombinant genotypes over many generations.
Furthermore, parentage analysis indicates genotype-by-environment
interactions for fitness, with the A. m. striatum - and A.
m. pseudomajus -like genotypes having an advantage in their home
territory. As there are no obvious difference in habitat or other
phenotypes across the hybrid zone, and given that pollinators are known
to discriminate between flowers based on colour, non-random foraging
behaviour by pollinators is an appealing explanation for these
differences in fitness. Statement about female fitness (in the core
only?) from \citet{Tastard2012}, but we
still don’t know much about male fitness. Parentage estimates reflect
the whole life cycle, which includes variation in mating success,
seedling establish and survival, and we are not able to distinguish
pollen and seed dispersal. As such, this is not ideal to investigate
mating patterns directly to properly characterise male fitness and
pollen dispersal.
In this study we reconstruct mating events between wild snapdragons in
the hybrid zone. We use a panel of open-pollinated seedlings of known
maternity collected in a natural hybrid zone and dense sampling of
possible sires. This differs from the pedigree because there is no seed
dispersal or establishment, so parentage reflects mating patterns
through pollen movement only. We build on previous methods to jointly
infer paternity, sibship relationships and the pollen dispersal kernel.
Use these results to examine the extent to which pollinators cause
assortative mating and differences in male fitness beyond what would be
expected due to local population structure. Finally we use simulations
to verify that these results are unlikely to be due to false positive
paternity assignment due to insufficient statistical power or missing
fathers. These results imply that pollinators are an important force
mediating selection on flower colour.
Materials and
Methods
Study
population