New methods
As genomic techniques are increasingly accessible, several methods can
contribute to the estimation of fitness and characterization of filial
generations in wild populations. For example, field-based pedigrees are
commonly used in studies of birds and mammals (e.g. Marr et al. 2002,
Martinig et al. 2020), and offer a promising perspective for other taxa
(e.g. plants, Ellstrand 214). Alternatively, parental line genotyping
has been used to identify admixed offspring (e.g. Bull & Sunnucks
2014), and even further discriminate among filial generations (e.g.
Fitzpatrick et al. 2016), allowing for fitness comparisons in systems
where individual-based datasets are impractical. More recently, new
statistical tools have been developed that enable accurate genetic
assignment of individuals into demes within genetically structured
metapopulation systems (e.g. Kuismin et al. 2020). In combination with
other field-based data, classification of individuals into immigrant,
residents, and several filial generations is possible (e.g. Saatoglu et
al. 2021). Therefore, these methods have the potential to enormously
contribute to the feasibility of heterosis studies in natural
populations. Furthermore, these methods can be combined with traditional
experimental approaches such as controlled crosses and reciprocal
transplants, significantly enriching the understanding of ancestry of
individuals in cross-sectional studies.
Genomic tools may allow further advancements of the field by enabling
field studies to assign continuous hybrid categorizations without
explicit knowledge of filial generation categories (e.g. Aase et al.
2022). For instance, longevity and reproductive success were shown to
positively correlate with Buerkle’s hybrid index (Buerkle 2005) in the
bighorn sheep (Ovis canadensis ; Miller et al. 2012). In turn,
although “pure” non-local individuals of the perennial plantArenaria grandiflora had higher fitness than “pure” locals,
admixtured individuals with higher proportions of locally-sourced
genetic composition presented the highest fitness, suggesting a complex,
non-linear, relationship between fitness and Buerkle’s hybrid index
(Zavodna et al. 2015). Moreover, genomic methods have been widely used
to estimate relationships between fitness and heterozygosity in
inbreeding depression studies. Notably, heterozygosity and Buerkle’s
hybrid indexes parallel the concepts of hybridization and source indexes
introduced by the line-cross theory (Box 1). Therefore, theoretical
developments elucidating the relationship between these indexes are
crucial, and will open new avenues of research by allowing the
application of line-cross theory, as well as its extensions
incorporating estimates of local adaptation (Schneemann et al. 2020), to
the study of wild populations.
Finally, because selection removes variation from the population,
fitness estimates may be positively biased, resulting in apparent
positive heterosis, due to the loss of less fit offspring before
estimates are recorded. Consequently, fitness observed in further
generations will result from a biased sample of the previous
generations’ genotypes (e.g. see Thompson et al. 2022a). The application
of line-cross theory in studies of wild populations, therefore, requires
that future theoretical developments incorporate changes in allele
frequencies across generations as to account for the effects of
selection when estimating the expected fitness of hybrid offspring.