Estimating ancestry and heterozygosity of hybrids using molecular markers

Background Hybridization, genetic mixture of distinct populations, gives rise to myriad recombinant genotypes. Characterizing the genomic composition of hybrids is critical for studies of hybrid zone dynamics, inheritance of traits, and consequences of hybridization for evolution and conservation. Hybrid genomes are often summarized either by an estimate of the proportion of alleles coming from each ancestral population or classification into discrete categories like F1, F2, backcross, or merely “hybrid” vs. “pure”. In most cases, it is not realistic to classify individuals into the restricted set of classes produced in the first two generations of admixture. However, the continuous ancestry index misses an important dimension of the genotype. Joint consideration of ancestry together with interclass heterozygosity (proportion of loci with alleles from both ancestral populations) captures all of the information in the discrete classification without the unrealistic assumption that only two generations of admixture have transpired. Methods I describe a maximum likelihood method for joint estimation of ancestry and interclass heterozygosity. I present two worked examples illustrating the value of the approach for describing variation among hybrid populations and evaluating the validity of the assumption underlying discrete classification. Results Naively classifying natural hybrids into the standard six line cross categories can be misleading, and false classification can be a serious problem for datasets with few molecular markers. My analysis underscores previous work showing that many (50 or more) ancestry informative markers are needed to avoid erroneous classification. Conclusion Although classification of hybrids might often be misleading, valuable inferences can be obtained by focusing directly on distributions of ancestry and heterozygosity. Estimating and visualizing the joint distribution of ancestry and interclass heterozygosity is an effective way to compare the genetic structure of hybrid populations and these estimates can be used in classic quantitative genetic methods for assessing additive, dominant, and epistatic genetic effects on hybrid phenotypes and fitness. The methods are implemented in a freely available package “HIest” for the R statistical software ( http://cran.r-project.org/web/packages/HIest/index.html webcite)

Alternative forms for genomic clines

Understanding factors regulating hybrid fitness and gene exchange is a major research challenge for evolutionary biology. Genomic cline analysis has been used to evaluate alternative patterns of introgression, but only two models have been used widely and the approach has generally lacked a hypothesis testing framework for distinguishing effects of selection and drift. I propose two alternative cline models, implement multivariate outlier detection to identify markers associated with hybrid fitness, and simulate hybrid zone dynamics to evaluate the signatures of different modes of selection. Analysis of simulated data shows that previous approaches are prone to false positives (multinomial regression) or relatively insensitive to outlier loci affected by selection (Barton\u27s concordance). The new, theory-based logit-logistic cline model is generally best at detecting loci affecting hybrid fitness. Although some generalizations can be made about different modes of selection, there is no one-to-one correspondence between pattern and process. These new methods will enhance our ability to extract important information about the genetics of reproductive isolation and hybrid fitness. However, much remains to be done to relate statistical patterns to particular evolutionary processes. The methods described here are implemented in a freely available package “HIest” for the R statistical software (CRAN; http://cran.r-project.org/). DOI: 10.1002/ece3.60

Frequency-dependent selection by wild birds promotes polymorphism in model salamanders

<p>Abstract</p> <p>Background</p> <p>Co-occurrence of distinct colour forms is a classic paradox in evolutionary ecology because both selection and drift tend to remove variation from populations. Apostatic selection, the primary hypothesis for maintenance of colour polymorphism in cryptic animals, proposes that visual predators focus on common forms of prey, resulting in higher survival of rare forms. Empirical tests of this frequency-dependent foraging hypothesis are rare, and the link between predator behaviour and maintenance of variation in prey has been difficult to confirm. Here, we show that predatory birds can act as agents of frequency-dependent selection on terrestrial salamanders. Polymorphism for presence/absence of a dorsal stripe is widespread in many salamander species and its maintenance is a long-standing mystery.</p> <p>Results</p> <p>We used realistic food-bearing model salamanders to test whether selection by wild birds maintains a stripe/no-stripe polymorphism. In experimental manipulations, whichever form was most common was most likely to be attacked by ground-foraging birds, resulting in a survival advantage for the rare form.</p> <p>Conclusion</p> <p>This experiment demonstrates that frequency-dependent foraging by wild birds can maintain colour polymorphism in cryptic prey.</p

Transgressive Hybdrids as Hopeful Monsters

The origin of novelty is a critical subject for evolutionary biologists. Early geneticists speculated about the sudden appearance of new species via special macromutations, epitomized by Goldschmidt’s infamous “hopeful monster”. Although these ideas were easily dismissed by the insights of the Modern Synthesis, a lingering fascination with the possibility of sudden, dramatic change has persisted. Recent work on hybridization and gene exchange suggests an underappreciated mechanism for the sudden appearance of evolutionary novelty that is entirely consistent with the principles of modern population genetics. Genetic recombination in hybrids can produce transgressive phenotypes, “monstrous” phenotypes beyond the range of parental populations. Transgressive phenotypes can be products of epistatic interactions or additive effects of multiple recombined loci. We compare several epistatic and additive models of transgressive segregation in hybrids and find that they are special cases of a general, classic quantitative genetic model. The Dobzhansky-Muller model predicts “hopeless” monsters, sterile and inviable transgressive phenotypes. The Bateson model predicts “hopeful” monsters with fitness greater than either parental population. The complementation model predicts both. Transgressive segregation after hybridization can rapidly produce novel phenotypes by recombining multiple loci simultaneously. Admixed populations will also produce many similar recombinant phenotypes at the same time, increasing the probability that recombinant “hopeful monsters” will establish true-breeding evolutionary lineages. Recombination is not the only (or even most common) process generating evolutionary novelty, but might be the most credible mechanism for sudden appearance of new forms DOI: 10.1007/s11692-012-9209-

Frequency-dependent selection by wild birds promotes polymorphism in model salamanders

Background Co-occurrence of distinct colour forms is a classic paradox in evolutionary ecology because both selection and drift tend to remove variation from populations. Apostatic selection, the primary hypothesis for maintenance of colour polymorphism in cryptic animals, proposes that visual predators focus on common forms of prey, resulting in higher survival of rare forms. Empirical tests of this frequency-dependent foraging hypothesis are rare, and the link between predator behaviour and maintenance of variation in prey has been difficult to confirm. Here, we show that predatory birds can act as agents of frequency-dependent selection on terrestrial salamanders. Polymorphism for presence/absence of a dorsal stripe is widespread in many salamander species and its maintenance is a long-standing mystery. Results We used realistic food-bearing model salamanders to test whether selection by wild birds maintains a stripe/no-stripe polymorphism. In experimental manipulations, whichever form was most common was most likely to be attacked by ground-foraging birds, resulting in a survival advantage for the rare form. Conclusion This experiment demonstrates that frequency-dependent foraging by wild birds can maintain colour polymorphism in cryptic prey

Estimating ancestry and heterozygosity of hybrids using molecular markers

Abstract Background Hybridization, genetic mixture of distinct populations, gives rise to myriad recombinant genotypes. Characterizing the genomic composition of hybrids is critical for studies of hybrid zone dynamics, inheritance of traits, and consequences of hybridization for evolution and conservation. Hybrid genomes are often summarized either by an estimate of the proportion of alleles coming from each ancestral population or classification into discrete categories like F1, F2, backcross, or merely “hybrid” vs. “pure”. In most cases, it is not realistic to classify individuals into the restricted set of classes produced in the first two generations of admixture. However, the continuous ancestry index misses an important dimension of the genotype. Joint consideration of ancestry together with interclass heterozygosity (proportion of loci with alleles from both ancestral populations) captures all of the information in the discrete classification without the unrealistic assumption that only two generations of admixture have transpired. Methods I describe a maximum likelihood method for joint estimation of ancestry and interclass heterozygosity. I present two worked examples illustrating the value of the approach for describing variation among hybrid populations and evaluating the validity of the assumption underlying discrete classification. Results Naively classifying natural hybrids into the standard six line cross categories can be misleading, and false classification can be a serious problem for datasets with few molecular markers. My analysis underscores previous work showing that many (50 or more) ancestry informative markers are needed to avoid erroneous classification. Conclusion Although classification of hybrids might often be misleading, valuable inferences can be obtained by focusing directly on distributions of ancestry and heterozygosity. Estimating and visualizing the joint distribution of ancestry and interclass heterozygosity is an effective way to compare the genetic structure of hybrid populations and these estimates can be used in classic quantitative genetic methods for assessing additive, dominant, and epistatic genetic effects on hybrid phenotypes and fitness. The methods are implemented in a freely available package “HIest” for the R statistical software (http://cran.r-project.org/web/packages/HIest/index.html).</p

iteRates: An R Package for Implementing a Parametric Rate Comparison on Phylogenetic Trees

Patterns of diversification rate variation detected in phylogenetic hypotheses are frequently used to infer historical, ecological, and evolutionary processes. The parametric rate comparison (PRC) is a method for detecting rate variation in trees that models branch lengths as random variables drawn from familiar statistical distributions. iteRates is a library of functions for the R statistical computing environment for implementing PRC on phylogenetic trees. Here, we describe some of the functions in iteRates for subtree identification, tree manipulation, applying the PRC and K-clades PRC analyses, and conducting a whole-tree randomization test

Isolation by distance, local adaptation, and fortuitous coincidence of geo-political boundaries with spatial-genetic clusters in southern Bog Turtles

Conservation strategies are often implemented within the jurisdiction of an administrative unit, such as a state or federal agency; however, boundaries between these units may or may not reflect biologically meaningful distinctions. Population genomic data provide a useful way to objectively assess whether boundaries of administrative units coincide with natural population structure, as well as compare future management scenarios within and among said units. Here we used 2658 SNPs generated by a triple-digest reduced representation library preparation method from 171 individuals to determine if genetic population structure of Bog Turtles corresponds with political boundaries. We also estimated gentetic diversity within populations pertinent to setting management priorities and tested for genetic signatures consistent with local adaptation as a preliminary step to assess translocation risk. We found that genetic differentiation among populations was strongly predicted by geographic distance. Fortuitously, the patchy distribution of remaining Bog Turtle sites results in spatial-genetic clusters that do correspond with state boundaries. We observed low genetic diversity within populations and several instances where the census size exceeded our estimates of effective population size. Lastly, we detected 20 outlier loci consistent with signatures of local adaptation, suggesting that outbreeding depression may be a risk in some translocation options. Our approach allowed us to improve population parameter estimates for the federally threatened Bog Turtle to address key recovery plan objectives, some of which had not been addressed previously

Retention of low-fitness genotypes over six decades of admixture between native and introduced tiger salamanders

<p>Abstract</p> <p>Background</p> <p>Introductions of non-native tiger salamanders into the range of California tiger salamanders have provided a rare opportunity to study the early stages of secondary contact and hybridization. We produced first- and second-generation hybrid salamanders in the lab and measured viability among these early-generation hybrid crosses to determine the strength of the initial barrier to gene exchange. We also created contemporary-generation hybrids in the lab and evaluated the extent to which selection has affected fitness over approximately 20 generations of admixture. Additionally, we examined the inheritance of quantitative phenotypic variation to better understand how evolution has progressed since secondary contact.</p> <p>Results</p> <p>We found significant variation in the fitness of hybrids, with non-native backcrosses experiencing the highest survival and F2 hybrids the lowest. Contemporary-generation hybrids had similar survival to that of F2 families, contrary to our expectation that 20 generations of selection in the wild would eliminate unfit genotypes and increase survival. Hybrid survival clearly exhibited effects of epistasis, whereas size and growth showed mostly additive genetic variance, and time to metamorphosis showed substantial dominance.</p> <p>Conclusions</p> <p>Based on first- and second- generation cross types, our results suggest that the initial barrier to gene flow between these two species was relatively weak, and subsequent evolution has been generally slow. The persistence of low-viability recombinant hybrid genotypes in some contemporary populations illustrates that while hybridization can provide a potent source of genetic variation upon which natural selection can act, the sorting of fit from unfit gene combinations might be inefficient in highly admixed populations. Spatio-temporal fluctuation in selection or complex genetics has perhaps stalled adaptive evolution in this system despite selection for admixed genotypes within generations.</p