Anthropogenic Change and the Process of Speciation.

Anthropogenic impacts on the environment alter speciation processes by affecting both geographical contexts and selection patterns on a worldwide scale. Here we review evidence of these effects. We find that human activities often generate spatial isolation between populations and thereby promote genetic divergence but also frequently cause sudden secondary contact and hybridization between diverging lineages. Human-caused environmental changes produce new ecological niches, altering selection in diverse ways that can drive diversification; but changes also often remove niches and cause extirpations. Human impacts that alter selection regimes are widespread and strong in magnitude, ranging from local changes in biotic and abiotic conditions to direct harvesting to global climate change. Altered selection, and evolutionary responses to it, impacts early-stage divergence of lineages, but does not necessarily lead toward speciation and persistence of separate species. Altogether, humans both promote and hinder speciation, although new species would form very slowly relative to anthropogenic hybridization, which can be nearly instantaneous. Speculating about the future of speciation, we highlight two key conclusions: (1) Humans will have a large influence on extinction and "despeciation" dynamics in the short term and on early-stage lineage divergence, and thus potentially speciation in the longer term, and (2) long-term monitoring combined with easily dated anthropogenic changes will improve our understanding of the processes of speciation. We can use this knowledge to preserve and restore ecosystems in ways that promote (re-)diversification, increasing future opportunities of speciation and enhancing biodiversity.

Co-evolution of dormancy and dispersal in spatially autocorrelated landscapes.

The evolution of dispersal can be driven by spatial processes, such as landscape structure, and temporal processes, such as disturbance. Dormancy, or dispersal in time, is generally thought to evolve in response to temporal processes. In spite of broad empirical and theoretical evidence of trade-offs between dispersal and dormancy, we lack evidence that spatial structure can drive the evolution of dormancy. Here, we develop a simulation-based model of the joint evolution of dispersal and dormancy in spatially heterogeneous landscapes. We show that dormancy and dispersal are each favored under different landscape conditions, but not simultaneously under any of the conditions we tested. We further show that, when dispersal distances are short, dormancy can evolve directly in response to landscape structure. In this case, selection is primarily driven by benefits associated with avoiding kin competition. Our results are similar in both highly simplified and realistically complex landscapes.

Different factors limit early- and late-season windows of opportunity for monarch development.

Seasonal windows of opportunity are intervals within a year that provide improved prospects for growth, survival, or reproduction. However, few studies have sufficient temporal resolution to examine how multiple factors combine to constrain the seasonal timing and extent of developmental opportunities. Here, we document seasonal changes in milkweed (Asclepias fascicularis)-monarch (Danaus plexippus) interactions with high resolution throughout the last three breeding seasons prior to a precipitous single-year decline in the western monarch population. Our results show early- and late-season windows of opportunity for monarch recruitment that were constrained by different combinations of factors. Early-season windows of opportunity were characterized by high egg densities and low survival on a select subset of host plants, consistent with the hypothesis that early-spring migrant female monarchs select earlier-emerging plants to balance a seasonal trade-off between increasing host plant quantity and decreasing host plant quality. Late-season windows of opportunity were coincident with the initiation of host plant senescence, and caterpillar success was negatively correlated with heatwave exposure, consistent with the hypothesis that late-season windows were constrained by plant defense traits and thermal stress. Throughout this study, climatic and microclimatic variations played a foundational role in the timing and success of monarch developmental windows by affecting bottom-up, top-down, and abiotic limitations. More exposed microclimates were associated with higher developmental success during cooler conditions, and more shaded microclimates were associated with higher developmental success during warmer conditions, suggesting that habitat heterogeneity could buffer the effects of climatic variation. Together, these findings show an important dimension of seasonal change in milkweed-monarch interactions and illustrate how different biotic and abiotic factors can limit the developmental success of monarchs across the breeding season. These results also suggest the potential for seasonal sequences of favorable or unfavorable conditions across the breeding range to strongly affect monarch population dynamics.

Adult facilitation becomes competition as juvenile soapberry bugs age.

Intraspecific interactions can change from facilitative to competitive depending on the organism's ontogeny. In plant-feeding insects, host plant defenses can be strengthened or weakened by insect feeding and can therefore be important for determining whether two insects feeding on the same plant help or harm each other's fitness. Here, I conducted two experiments looking at the direct effect of a physical seed defense and the role of intraspecific facilitation in reducing the effects of that defense for juveniles of the red-shouldered soapberry bug. I demonstrate that juveniles are severely inhibited by the tough seed coat of their host plant, leading to high mortality early in development. Adults, in contrast, can create holes through which younger individuals could potentially feed. I manipulated whether or not seeds were fed on by adults on two host plant species: a well-defended native host and a poorly defended introduced host. Survival in the first week of development was dramatically improved by prior adult feeding, and this facilitation was stronger on the well-defended host plant. However, the benefits of prior adult feeding ceased after the first week of development and shifted to having a negative effect on survival, development time, and body size. These results indicate that ontogeny is a key factor determining the effects of plant defenses and the strength and direction of intraspecific interactions across multiple host plant species.

Species-specific, age-varying plant traits affect herbivore growth and survival.

Seasonal windows of opportunity represent intervals of time within a year during which organisms have improved prospects of achieving life history aims such as growth or reproduction, and may be commonly structured by temporal variation in abiotic factors, bottom-up factors, and top-down factors. Although seasonal windows of opportunity are likely to be common, few studies have examined the factors that structure seasonal windows of opportunity in time. Here, we experimentally manipulated host-plant age in two milkweed species (Asclepias fascicularis and Asclepias speciosa) in order to investigate the role of plant-species-specific and plant-age-varying traits on the survival and growth of monarch caterpillars (Danaus plexippus). We show that the two plant species showed diverging trajectories of defense traits with increasing age. These species-specific and age-varying host-plant traits significantly affected the growth and survival of monarch caterpillars through both resource quality- and quantity-based constraints. The effects of plant age on monarch developmental success were comparable to and sometimes larger than those of plant-species identity. We conclude that species-specific and age-varying plant traits are likely to be important factors with the potential to structure seasonal windows of opportunity for monarch development, and examine the implications of these findings for both broader patterns in the ontogeny of plant defense traits and the specific ecology of milkweed-monarch interactions in a changing world.

Seasonal windows of opportunity in milkweed-monarch interactions.

Many organisms experience seasonal windows of opportunity for growth and reproduction. These windows represent intervals in time when organisms experience improved prospects for advancing their life history objectives, constrained by the combined effects of seasonally variable biotic and abiotic conditions acting independently or in combination. Although seasonal windows of opportunity are likely to be widespread in nature, relatively few studies have conducted the repeated observations necessary to identify them or suggest the factors that structure them in time. Here, we present the results of three experimental studies conducted at different field sites in three different years in which we manipulated the phenology of monarch caterpillars (Danaus plexippus) throughout the growing season. The primary aims of these experiments were (1) to identify seasonal windows of opportunity for successful larval development on milkweed (Asclepias spp.), and (2) to suggest which factors are most likely to constrain these windows of opportunity in time. We found strong seasonal windows of opportunity in the developmental success of monarchs, with distinct periods of higher developmental prospects during each study year. We evaluated the role of seasonal variation in abiotic thermal stress, host plant density, host plant defensive traits, and natural enemy risk as potential factors that may limit seasonal windows of opportunity. By comparing the seasonal patterns of larval success and potential explanatory factors across all 3 yr, we find patterns that are consistent with seasonally variable abiotic conditions, host plant availability, host plant traits, and natural enemy risk factors. These results suggest the potential for seasonal variation in the factors that limit monarch larval development and population growth. More generally, this study also highlights the value of temporally explicit experimental studies that can identify and examine seasonal patterns in species interactions.

Local adaptation in dispersal in multi-resource landscapes.

The distribution of resources in space has important consequences for the evolution of dispersal-related traits. Dispersal moderates patterns of gene flow and, consequently, the potential for local adaptation to spatially differentiated resource types. We lack both models and experiments that evaluate how dispersal evolves in landscapes with multiple resources. Here, we investigate the evolution of dispersal in landscapes that contain two resource types that differ in their spatial autocorrelations. Individuals may possess ecological traits that give them a fitness advantage on one or the other resource. We find that resources differing in their spatial autocorrelation select for different optimal dispersal strategies and, further, that some multi-resource landscapes can support the stable coexistence of distinct dispersal strategies. Whether divergence in dispersal strategies between resource specialists occurs depends on the underlying structure of the resources and the degree of linkage between dispersal strategies and ecological specialization. This work indicates that the spatial autocorrelation of resources is an important factor in determining when evolutionary branching is likely to occur, and sheds light on when secondary isolating mechanisms should arise between locally adapted specialists.

Manipulation of insulin signaling phenocopies evolution of a host-associated polyphenism.

Plasticity, the capacity of an organism to respond to its environment, is thought to evolve through changes in development altering the integration of environmental cues. In polyphenism, a discontinuous plastic response produces two or more phenotypic morphs. Here we describe evolutionary change in wing polyphenism and its underlying developmental regulation in natural populations of the red-shouldered soapberry bug, Jadera haematoloma (Insecta: Hemiptera: Rhopalidae) that have adapted to a novel host plant. We find differences in the fecundity of morphs in both sexes and in adult expression of insulin signaling components in the gonads. Further, the plastic response of ancestral-state bugs can be shifted to resemble the reaction norm of derived bugs by the introduction of exogenous insulin or RNA interference targeting the insulin signaling component encoded by FoxO. These results suggest that insulin signaling may be one pathway involved in the evolution of this polyphenism, allowing adaptation to a novel nutritional environment.

Maladaptive Plasticity Masks the Effects of Natural Selection in the Red-Shouldered Soapberry Bug.

Natural selection can produce local adaptation, but local adaptation can be masked by maladaptive plasticity. Maladaptive plasticity may arise as a result of gene flow producing novel gene combinations that have not been exposed to selection. In the 1980s, populations of the red-shouldered soapberry bug (Jadera haematoloma) were locally adapted to feed on the seeds of a native host plant and an introduced host plant; by 2014, local differentiation in beak length had been lost, likely as a consequence of increased gene flow. In this study, I assess the relative contributions of natural selection and plasticity to beak length on these two hosts. I confirm the earlier hypothesis that the host plant seedpod drives divergent natural selection on beak length. I then demonstrate that the proximate cause of the loss of observable differentiation in beak length is maladaptive plasticity, which masks persistent genetic differences between host-associated populations. Maladaptive plasticity is highest in areas where the two plants co-occur; in combination with historical measures of plasticity in hybrids, this indicates that maladaptive plasticity may be a consequence of ongoing gene flow. Although natural selection produced locally adapted genotypes in soapberry bugs, maladaptive plasticity is masking phenotypic differences between populations in nature.

Adaptation to an invasive host is driving the loss of a native ecotype.

Locally adapted populations are often used as model systems for the early stages of ecological speciation, but most of these young divergent populations will never become complete species. The maintenance of local adaptation relies on the strength of natural selection overwhelming the homogenizing effects of gene flow; however, this balance may be readily upset in changing environments. Here I show that soapberry bugs (Jadera haematoloma) have lost adaptations to their native host plant (Cardiospermum corindum) and are regionally specializing on an invasive host (Koelreuteria elegans), collapsing a classic and well-documented example of local adaptation. All populations that were adapted to the native host-including those still found on that host today-are now better adapted to the invasive host in multiple phenotypes. Weak differentiation remains in two traits, suggesting that homogenization across the region is incomplete. This study highlights the potential for adaptation to invasive species to disrupt native communities by swamping adaptation to native conditions through maladaptive gene flow.