Adam H. Porter

THE PONTIA DAPLIDICE-EDUSA HYBRID ZONE IN NORTHWESTERN ITALY

The pierid butterflies Pontia daplidice and P. edusa, parapatrically distributed in southern Europe, have very similar morphologies and life histories, but show fixed differences at four allozyme markers. We sampled these allozymes in a 28‐population transect north of Genoa in Italy, through the hybrid zone where these taxa meet. We used the numerical techniques developed for hybrid zone analysis to study the patterns of genetic differentiation and their underlying evolutionary causes. The hybrid zone is characterized by a very short and steep central region, flanked by broad tails of introgression extended up to 100 km in either direction. From mean two‐locus disequilibium of D = 0.148 (maximum‐likelihood two‐unit support limits 0.139‐0.153), and after accounting for minor differences in the center locations of the single‐locus clines, which act to bias the dispersal estimate, we estimated a dispersal rate of σ = 4.4 (3.7‐5.5) km/gen1/2. The effective selection needed to maintain the steep central portion is strong, 0.47 < s∗ < 0.64, when combined over potential intrinsic (genetic background) and extrinsic (ecological) sources of selection. The clines in allozyme loci showed variation that was significantly different between the most divergent shapes, and the differences are attributable to different degrees of introgression on the edusa side of the zone. The average selection acting on individual allozyme loci was high at s∗∗∗e  1.5%, but because of the narrowness of the central region of the cline, we suspect that this estimate is somewhat biased by selection on loci closely linked to the allozyme markers. A common question for taxa that show fixed allozyme differences in parapatry is whether or not they are genetically isolated. A fairly general measure of genetic isolation across hybrid zones is the time, T, that it takes a neutral allele to cross the hybrid zone and recombine into the opposite genetic background, given by T = (β/σ)2, where β is the barrier strength of the hybrid zone. Genetic isolation in the Pontia zone is weak, with T  25 generations for most allozyme markers. By this measure, populations of daplidice and edusa on opposite sides of the hybrid zone share more identical‐by‐descent alleles than do populations of phenotypically pure daplidice in, say, France and Morocco. Accordingly, we think it best for systematists to consider edusa as a well‐marked subspecies of P. daplidice.

SPECIATION DESPITE GENE FLOW WHEN DEVELOPMENTAL PATHWAYS EVOLVE

Abstract.— Evolutionary biologists assume that species formation requires a drastic reduction in gene exchange between populations, but the rate sufficient to prevent speciation is unknown. To study speciation, we use a new class of population genetic models that incorporate simple developmental genetic rules, likely present in all organisms, to construct the phenotype. When we allow replicate populations to evolve in parallel to a new, shared optimal phenotype, often their hybrids acquire poorly regulated phenotypes: Dobzhansky‐Muller incompatibilities arise and postzygotic reproductive isolation evolves. Here we show that, although gene exchange does inhibit this process, it is the proportion of migrants exchanged (m) rather than the number of migrants (Nm) that is critical, and rates as high as 16 individuals exchanged per generation still permit the evolution of postzygotic isolation. Stronger directional selection counters the inhibitory effect of gene flow, increasing the speciation probability. We see similar results when populations in a standard two‐locus, two‐allele Dobzhansky‐Muller model are subject to simultaneous directional selection and gene flow. However, in developmental pathway models with more than two loci, gene flow is more able to impede speciation. Genetic incompatibilities arise as frequent by‐products of adaptive evolution of traits determined by regulatory pathways, something that does not occur when phenotypes are modeled using the standard, additive genetic framework. Development therefore not only constrains the microevolutionary process, it also facilitates the interactions among genes and gene products that make speciation more likely–even in the face of strong gene flow.

Evolution of branched regulatory genetic pathways: directional selection on pleiotropic loci accelerates developmental system drift

Developmental systems are regulated by a web of interacting loci. One common and useful approach in studying the evolution of development is to focus on classes of interacting elements within these systems. Here, we use individual-based simulations to study the evolution of traits controlled by branched developmental pathways involving three loci, where one locus regulates two different traits. We examined the system under a variety of selective regimes. In the case where one branch was under stabilizing selection and the other under directional selection, we observed “developmental system drift”: the trait under stabilizing selection showed little phenotypic change even though the loci underlying that trait showed considerable evolutionary divergence. This occurs because the pleiotropic locus responds to directional selection and compensatory mutants are then favored in the pathway under stabilizing selection. Though developmental system drift may be caused by other mechanisms, it seems likely that it is accelerated by the same underlying genetic mechanism as that producing the Dobzhansky–Muller incompatibilities that lead to speciation in both linear and branched pathways. We also discuss predictions of our model for developmental system drift and how different selective regimes affect probabilities of speciation in the branched pathway system.

Modeling Range Dynamics In Heterogeneous Landscapes: Invasion Of The Hemlock Woolly Adelgid In Eastern North America

Range expansion by native and exotic species will continue to be a major component of global change. Anticipating the potential effects of changes in species distributions requires models capable of forecasting population spread across realistic, heterogeneous landscapes and subject to spatiotemporal variability in habitat suitability. Several decades of theory and model development, as well as increased computing power and availability of fine-resolution GIS data, now make such models possible. Still unanswered, however, is the question of how well this new generation of dynamic models will anticipate range expansion. Here we develop a spatially explicit stochastic model that combines dynamic dispersal and population processes with fine-resolution maps characterizing spatiotemporal heterogeneity in climate and habitat to model range expansion of the hemlock woolly adelgid (HWA; Adelges tsugae). We parameterize this model using multiyear data sets describing population and dispersal dynamics of HWA and apply it to eastern North America over a 57-year period (1951-2008). To evaluate the model, the observed pattern of spread of HWA during this same period was compared to model predictions. Our model predicts considerable heterogeneity in the risk of HWA invasion across space and through time, and it suggests that spatiotemporal variation in winter temperature, rather than hemlock abundance, exerts a primary control on the spread of HWA. Although the simulations generally matched the observed current extent of the invasion of HWA and patterns of anisotropic spread, it did not correctly predict when HWA was observed to arrive in different geographic regions. We attribute differences between the modeled and observed dynamics to an inability to capture the timing and direction of long-distance dispersal events that substantially affected the ensuing pattern of spread.

Toward a new synthesis: Population genetics and evolutionary developmental biology

Despite the recent synthesis of developmental genetics and evolutionary biology, current theories of adaptation are still strictly phenomenological and do not yet consider the implications of how phenotypes are constructed from genotypes. Given the ubiquity of regulatory genetic pathways in developmental processes, we contend that study of the population genetics of these pathways should become a major research program. We discuss the role divergence in regulatory developmental genetic pathways may play in speciation, focusing on our theoretical and computational investigations. We also discuss the population genetics of molecular co-option, arguing that mutations of large effect are not needed for co-option. We offer a prospectus for future research, arguing for a new synthesis of the population genetics of development.

Persistence and Inheritance of Costs of Resistance to Imidacloprid in Colorado Potato Beetle

Abstract Reduced fitness among resistant versus susceptible individuals slows resistance evolution and makes it easier to manage. A loss of resistance costs could indicate novel adaptations or mutations contributing to resistance. We measured costs of resistance to imidacloprid in a Massachusetts resistant population compared with a Massachusetts susceptible population in 1999 in terms of fecundity, hatching success, egg development time, and sprint speed. Resistance was additive and seemed to be polygenic with high heritability. The fecundity cost appeared overdominant in 1999, and the hatch rate cost was partly recessive in 1999, but neither was significantly different from dominant or recessive. In 2004, we repeated our measures of resistance costs in Massachusetts in terms of fecundity and hatching success, and we added a new resistant population from Maine. In 2005, we compared development time of Maine resistant and the laboratory susceptible colony eggs. Significant fecundity costs of resistance were found in both population in both 1999 and 2004, and significant egg developmental time costs were found in 1999 and 2005. However, the hatching success costs of resistance were significant in 1999 and not apparent in 2004, suggesting some modification or replacement of the resistance genes in the intervening time.

Survey for Winter Moth (Lepidoptera: Geometridae) in Northeastern North America with Pheromone-Baited Traps and Hybridization with the Native Bruce Spanworm (Lepidoptera: Geometridae)

ABSTRACT We used pheromone-baited traps to survey the distribution of winter moth, Operophtera brumata (L.) (Lepidoptera: Geometridae), a new invasive defoliator from Europe in eastern New England. The traps also attracted Bruce spanworm, Operophtera bruceata (Hulst) (Lepidoptera: Geometridae), native to North America. We distinguished between the two species by examining male genitalia and sequencing the mitochondrial cytochrome oxidase subunit 1 (COI) gene, the DNA barcoding region. In 2005, we recovered winter moths at sites stretching from eastern Long Island, southeastern Connecticut, all of Rhode Island, eastern Massachusetts, coastal New Hampshire, and southern coastal Maine. At sites further west and north we captured only Bruce spanworm. In 2006, we confirmed that both winter moth and Bruce spanworm are present in Nova Scotia and in coastal Maine, but only Bruce spanworm was recovered in coastal New Brunswick, Canada; Pennsylvania; Vermont; or Quebec City, Canada. In 2007, we collected Bruce spanworm, but no winter moths, in New Brunswick and the interior areas of Maine, New Hampshire, and New York. Winter moth and Brace spanworm differed in the COI sequence by 7.45% of their nucleotides. The prevalence of intermediate genitalia in the zone of overlap suggested that hybridization between the two species may be occurring. To confirm the presence of hybrids, we sequenced the nuclear gene, glucose-6phosphate dehydrogenase (G6PD). We identified six nucleotides that routinely distinguished winter moth and Bruce spanworm, of which three were always diagnostic. We showed that eggs produced by hybridizing the two species in the laboratory contained copies of both species at these six sites. We found that most of the moths collected in the field with intermediate genitalia had winter moth CO1 and G6PD sequences and thus were not hybrids (or at least F1 hybrids). We found three hybrids out of 158 moths with intermediate genitalia in the region where both species were caught. We conclude that hybrids occur in nature, but are not as common as previously reported. Introgression of genes between the two species may still be significant.

Ecological boundary detection using Bayesian areal wombling.

The study of ecological boundaries and their dynamics is of fundamental importance to much of ecology, biogeography, and evolution. Over the past two decades, boundary analysis (of which wombling is a subfield) has received considerable research attention, resulting in multiple approaches for the quantification of ecological boundaries. Nonetheless, few methods have been developed that can simultaneously (1) analyze spatially homogenized data sets (i.e., areal data in the form of polygons rather than point-reference data); (2) account for spatial structure in these data and uncertainty associated with them; and (3) objectively assign probabilities to boundaries once detected. Here we describe the application of a Bayesian hierarchical framework for boundary detection developed in public health, which addresses these issues but which has seen limited application in ecology. As examples, we analyze simulated spread data and the historic pattern of spread of an invasive species, the hemlock woolly adelgid (Adelges tsugae), using county-level summaries of the year of first reported infestation and several covariates potentially important to influencing the observed spread dynamics. Bayesian areal wombling is a promising approach for analyzing ecological boundaries and dynamics related to changes in the distributions of native and invasive species.

A test for deviation from island-model population structure

The neutral island model forms the basis for several estimation models that relate patterns of genetic structure to microevolutionary processes. Estimates of gene flow are often based on this model and may be biased when the models assumptions are violated. An appropriate test for violations is to compare FST scores for individual loci to a null distribution based on the average FST taken over multiple loci. A parametric bootstrap method is described here based on Wrights β‐distribution to generate null distributions of FST for each locus. These null distributions account for error introduced by sampling populations, individuals and loci, and also biological sources of error, including variable alleles/locus and inbreeding. Confidence limits can be obtained directly from these distributions. Significant deviations from the island model may be the result of selection, deviations from the island models migration pattern, nonequilibrium conditions, or other deviations from island‐model assumptions. Only strong biases are likely to be detected because of the inherently large sampling variation of FST. Nevertheless, a coefficient, Nb, describing bias in the spread of the β‐distribution in units comparable to the gene flow parameter, Nm, can be obtained for each locus. In samples from populations of the butterfly Coenonympha tullia, the loci Idh‐1, Mdh‐1, Pgi and Pgm showed significantly lower FST than expected.

Hybrid Incompatibility Arises in a Sequence-Based Bioenergetic Model of Transcription Factor Binding

Postzygotic isolation between incipient species results from the accumulation of incompatibilities that arise as a consequence of genetic divergence. When phenotypes are determined by regulatory interactions, hybrid incompatibility can evolve even as a consequence of parallel adaptation in parental populations because interacting genes can produce the same phenotype through incompatible allelic combinations. We explore the evolutionary conditions that promote and constrain hybrid incompatibility in regulatory networks using a bioenergetic model (combining thermodynamics and kinetics) of transcriptional regulation, considering the bioenergetic basis of molecular interactions between transcription factors (TFs) and their binding sites. The bioenergetic parameters consider the free energy of formation of the bond between the TF and its binding site and the availability of TFs in the intracellular environment. Together these determine fractional occupancy of the TF on the promoter site, the degree of subsequent gene expression and in diploids, and the degree of dominance among allelic interactions. This results in a sigmoid genotype–phenotype map and fitness landscape, with the details of the shape determining the degree of bioenergetic evolutionary constraint on hybrid incompatibility. Using individual-based simulations, we subjected two allopatric populations to parallel directional or stabilizing selection. Misregulation of hybrid gene expression occurred under either type of selection, although it evolved faster under directional selection. Under directional selection, the extent of hybrid incompatibility increased with the slope of the genotype–phenotype map near the derived parental expression level. Under stabilizing selection, hybrid incompatibility arose from compensatory mutations and was greater when the bioenergetic properties of the interaction caused the space of nearly neutral genotypes around the stable expression level to be wide. F2’s showed higher hybrid incompatibility than F1’s to the extent that the bioenergetic properties favored dominant regulatory interactions. The present model is a mechanistically explicit case of the Bateson–Dobzhansky–Muller model, connecting environmental selective pressure to hybrid incompatibility through the molecular mechanism of regulatory divergence. The bioenergetic parameters that determine expression represent measurable properties of transcriptional regulation, providing a predictive framework for empirical studies of how phenotypic evolution results in epistatic incompatibility at the molecular level in hybrids.