Understanding the evolutionary dynamics of inbreeding and inbreeding depression requires unbiased estimation of inbreeding depression across diverse mating systems. However, studies estimating inbreeding depression often measure inbreeding with error, for example, based on pedigree data derived from observed parental behavior that ignore paternity error stemming from multiple mating. Such paternity error causes error in estimated coefficients of inbreeding (f) and reproductive success and could bias estimates of inbreeding depression. We used complete "apparent" pedigree data compiled from observed parental behavior and analogous "actual" pedigree data comprising genetic parentage to quantify effects of paternity error stemming from extra-pair reproduction on estimates of f, reproductive success, and inbreeding depression in free-living song sparrows (Melospiza melodia). Numerous studies have shown that, in normally outbreeding organisms, inbred offspring resulting from matings among relatives are typically less fit than outbred offspring resulting from matings * These authors contributed equally to this work. Paternity error caused widespread error in estimates of
Inbreeding depression, the deterioration in mean trait value in progeny of related parents, is a fundamental quantity in genetics, evolutionary biology, animal and plant breeding, and conservation biology. The magnitude of inbreeding depression can be quantified by the inbreeding load, typically measured in numbers of lethal equivalents, a population genetic quantity that allows for comparisons between environments, populations or species. However, there is as yet no quantitative assessment of which combinations of statistical models and metrics of inbreeding can yield such estimates. Here, we review statistical models that have been used to estimate inbreeding load and use population genetic simulations to investigate how unbiased estimates can be obtained using genomic and pedigree‐based metrics of inbreeding. We use simulated binary viability data (i.e., dead versus alive) as our example, but the concepts apply to any trait that exhibits inbreeding depression. We show that the increasingly popular generalized linear models with logit link do not provide comparable and unbiased population genetic measures of inbreeding load, independent of the metric of inbreeding used. Runs of homozygosity result in unbiased estimates of inbreeding load, whereas inbreeding measured from pedigrees results in slight overestimates. Due to widespread use of models that do not yield unbiased measures of the inbreeding load, some estimates in the literature cannot be compared meaningfully. We surveyed the literature for reliable estimates of the mean inbreeding load from wild vertebrate populations and found an average of 3.5 haploid lethal equivalents for survival to sexual maturity. To obtain comparable estimates, we encourage researchers to use generalized linear models with logarithmic links or maximum‐likelihood estimation of the exponential equation, and inbreeding coefficients calculated from runs of homozygosity, provided an assembled reference genome of sufficient quality and enough genetic marker data are available.
Extra-pair reproduction is widely hypothesized to allow females to avoid inbreeding with related socially paired males. Consequently, numerous field studies have tested the key predictions that extra-pair offspring are less inbred than females’ alternative within-pair offspring, and that the probability of extra-pair reproduction increases with a female's relatedness to her socially paired male. However, such studies rarely measure inbreeding or relatedness sufficiently precisely to detect subtle effects, or consider biases stemming from failure to observe inbred offspring that die during early development. Analyses of multigenerational song sparrow (Melospiza melodia) pedigree data showed that most females had opportunity to increase or decrease the coefficient of inbreeding of their offspring through extra-pair reproduction with neighboring males. In practice, observed extra-pair offspring had lower inbreeding coefficients than females’ within-pair offspring on average, while the probability of extra-pair reproduction increased substantially with the coefficient of kinship between a female and her socially paired male. However, simulations showed that such effects could simply reflect bias stemming from inbreeding depression in early offspring survival. The null hypothesis that extra-pair reproduction is random with respect to kinship therefore cannot be definitively rejected in song sparrows, and existing general evidence that females avoid inbreeding through extra-pair reproduction requires reevaluation given such biases.
The Southeast Asian Sunda archipelago harbors a rich biodiversity with a substantial proportion of endemic species. The evolutionary history of these species has been drastically influenced by environmental forces, such as fluctuating sea levels, climatic changes, and severe volcanic activities. Orangutans (genus: Pongo), the only Asian great apes, are well suited to study the relative impact of these forces due to their well-documented behavioral ecology, strict habitat requirements, and exceptionally slow life history. We investigated the phylogeographic patterns and evolutionary history of orangutans in the light of the complex geological and climatic history of the Sunda archipelago. Our study is based on the most extensive genetic sampling to date, covering the entire range of extant orangutan populations. Using data from three mitochondrial DNA (mtDNA) genes from 112 wild orangutans, we show that Sumatran orangutans, Pongo abelii, are paraphyletic with respect to Bornean orangutans (P. pygmaeus), the only other currently recognized species within this genus. The deepest split in the mtDNA phylogeny of orangutans occurs across the Toba caldera in northern Sumatra and, not as expected, between both islands. Until the recent past, the Toba region has experienced extensive volcanic activity, which has shaped the current phylogeographic patterns. Like their Bornean counterparts, Sumatran orangutans exhibit a strong, yet previously undocumented structuring into four geographical clusters. However, with 3.50 Ma, the Sumatran haplotypes have a much older coalescence than their Bornean counterparts (178 kya). In sharp contrast to the mtDNA data, 18 Y-chromosomal polymorphisms show a much more recent coalescence within Sumatra compared with Borneo. Moreover, the deep geographic structure evident in mtDNA is not reflected in the male population history, strongly suggesting male-biased dispersal. We conclude that volcanic activities have played an important role in the evolutionary history of orangutans and potentially of many other forest-dwelling Sundaland species. Furthermore, we demonstrate that a strong sex bias in dispersal can lead to conflicting patterns in uniparentally inherited markers even at a genus-wide scale, highlighting the need for a combined usage of maternally and paternally inherited marker systems in phylogenetic studies.
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