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  1. The idea that changing environmental conditions drive adaptive evolution is a pillar of evolutionary ecology. But, the opposite—that adaptive evolution alters ecological processes—has received far less attention yet is critical for eco-evolutionary dynamics. We assessed the ecological impact of divergent values in a key adaptive trait using 16 populations of the brown anole lizard ( Anolis sagrei ). Mirroring natural variation, we established islands with short- or long-limbed lizards at both low and high densities. We then monitored changes in lower trophic levels, finding that on islands with a high density of short-limbed lizards, web-spider densities decreased and plants grew more via an indirect positive effect, likely through an herbivore-mediated trophic cascade. Our experiment provides strong support for evolution-to-ecology connections in nature, likely closing an otherwise well-characterized eco-evolutionary feedback loop. 
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  2. Abstract

    Multivariate adaptation to climatic shifts may be limited by trait integration that causes genetic variation to be low in the direction of selection. However, strong episodes of selection induced by extreme climatic pressures may facilitate future population-wide responses if selection reduces trait integration and increases adaptive potential (i.e., evolvability). We explain this counter-intuitive framework for extreme climatic events in which directional selection leads to increased evolvability and exemplify its use in a case study. We tested this hypothesis in two populations of the lizard Anolis scriptus that experienced hurricane-induced selection on limb traits. We surveyed populations immediately before and after the hurricane as well as the offspring of post-hurricane survivors, allowing us to estimate both selection and response to selection on key functional traits: forelimb length, hindlimb length, and toepad area. The direct selection was parallel in both islands and strong in several limb traits. Even though overall limb integration did not change after the hurricane, both populations showed a non-significant tendency toward increased evolvability after the hurricane despite the direction of selection not being aligned with the axis of most variance (i.e., body size). The population with comparably lower between-limb integration showed a less constrained response to selection. Hurricane-induced selection, not aligned with the pattern of high trait correlations, likely conflicts with selection occurring during normal ecological conditions that favours functional coordination between limb traits, and would likely need to be very strong and more persistent to elicit a greater change in trait integration and evolvability. Future tests of this hypothesis should use G-matrices in a variety of wild organisms experiencing selection due to extreme climatic events.


    We surveyed populations of A. scriptus lizards, in two islands, before the hurricane, after the hurricane (estimate of survivors) and the offspring almost two years later. We hypothesized that the direction of hurricane-induced selection would be to reduce between-limb trait correlations, resulting in higher variation in the direction of selection (higher evolvability). We found that selection had a similar direction in both populations, but was likely not strong or persistent enough to change trait correlations. However, the population with lower limb trait correlations showed a response to selection more aligned with the direction of selection. Finally, both populations showed a tendency to increase evolvability after the hurricane.

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  3. Abstract

    As anthropogenic activities are increasing the frequency and severity of droughts, understanding whether and how fast populations can adapt to sudden changes in their hydric environment is critically important. Here, we capitalize on the introduction of the Cuban brown anole lizard (Anolis sagrei) in North America to assess the contemporary evolution of a widespread terrestrial vertebrate to an abrupt climatic niche shift. We characterized hydric balance in 30 populations along a large climatic gradient. We found that while evaporative and cutaneous water loss varied widely, there was no climatic cline, as would be expected under adaptation. Furthermore, the skin of lizards from more arid environments was covered with smaller scales, a condition thought to limit water conservation and thus be maladaptive. In contrast to environmental conditions, genome-averaged ancestry was a significant predictor of water loss. This was reinforced by our genome-wide association analyses, which indicated a significant ancestry-specific effect for water loss at one locus. Thus, our study indicates that the water balance of invasive brown anoles is dictated by an environment-independent introduction and hybridization history and highlights genetic interactions or genetic correlations as factors that might forestall adaptation. Alternative water conservation strategies, including behavioral mitigation, may influence the brown anole invasion success and require future examination.

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  4. Determining whether and how evolution is predictable is an important goal, particularly as anthropogenic disturbances lead to novel species interactions that could modify selective pres- sures. Here, we use a multigeneration field experiment with brown anole lizards (Anolis sagrei) to test hypotheses about the predictabil- ity of evolution. We manipulated the presence/absence of predators and competitors of A. sagrei across 16 islands in the Bahamas that had preexisting brown anole populations. Before the experiment and again after roughly five generations, we measured traits related to locomotor performance and habitat use by brown anoles and used double-digest restriction enzyme–associated DNA sequencing to estimate genome-wide changes in allele frequencies. Although previous work showed that predators and competitors had characteristic effects on brown anole behavior, diet, and population sizes, we found that evolutionary change at both phenotypic and genomic levels was difficult to forecast. Phenotypic changes were contingent on sex and hab- itat use, whereas genetic change was unpredictable and not measur- ably correlated with phenotypic changes, experimental treatments, or other environmental factors. Our work shows how differences in ecological context can alter evolutionary outcomes over short timescales and underscores the difficulty of forecasting evolutionary responses to multispecies interactions in natural conditions, even in a well-studied system with ample supporting ecological information. 
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  5. Abstract

    Introductions of invasive species to new environments often result in rapid rates of trait evolution. While in some cases these evolutionary transitions are adaptive and driven by natural selection, they can also result from patterns of genetic and phenotypic variation associated with the invasion history. Here, we examined the brown anole (Anolis sagrei), a widespread invasive lizard for which genetic data have helped trace the sources of non‐native populations. We focused on the dewlap, a complex signalling trait known to be subject to multiple selective pressures. We measured dewlap reflectance, pattern and size in 30 non‐native populations across the southeastern United States. As well, we quantified environmental variables known to influence dewlap signal effectiveness, such as canopy openness. Further, we used genome‐wide data to estimate genetic ancestry, perform association mapping and test for signatures of selection. We found that among‐population variation in dewlap characteristics was best explained by genetic ancestry. This result was supported by genome‐wide association mapping, which identified several ancestry‐specific loci associated with dewlap traits. Despite the strong imprint of this aspect of the invasion history on dewlap variation, we also detected significant relationships between dewlap traits and local environmental conditions. However, we found limited evidence that dewlap‐associated genetic variants have been subject to selection. Our study emphasizes the importance of genetic ancestry and admixture in shaping phenotypes during biological invasion, while leaving the role of selection unresolved, likely due to the polygenic genetic architecture of dewlaps and selection acting on many genes of small effect.

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  6. Abstract

    Invasive species can impact native populations through competition, predation, habitat alteration, and disease transmission, but also genetically through hybridization. Potential outcomes of hybridization span the continuum from extinction to hybrid speciation and can be further complicated by anthropogenic habitat disturbance. Hybridization between the native green anole lizard (Anolis carolinensis) and a morphologically similar invader (A. porcatus) in south Florida provides an ideal opportunity to study interspecific admixture across a heterogeneous landscape. We used reduced‐representation sequencing to describe introgression in this hybrid system and to test for a relationship between urbanization and non‐native ancestry. Our findings indicate that hybridization between green anole lineages was probably a limited, historic event, producing a hybrid population characterized by a diverse continuum of ancestry proportions. Genomic cline analyses revealed rapid introgression and disproportionate representation of non‐native alleles at many loci and no evidence for reproductive isolation between parental species. Three loci were associated with urban habitat characteristics; urbanization and non‐native ancestry were positively correlated, although this relationship did not remain significant when accounting for spatial nonindependence. Ultimately, our study demonstrates the persistence of non‐native genetic material even in the absence of ongoing immigration, indicating that selection favouring non‐native alleles can override the demographic limitation of low propagule pressure. We also note that not all outcomes of admixture between native and non‐native species should be considered intrinsically negative. Hybridization with ecologically robust invaders can lead to adaptive introgression, which may facilitate the long‐term survival of native populations otherwise unable to adapt to anthropogenically mediated global change.

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  7. Abstract

    Research conducted during the past two decades has demonstrated that biological invasions are excellent models of rapid evolution. Even so, characteristics of invasive populations such as a short time for recombination to assemble optimal combinations of alleles may occasionally limit adaptation to new environments. Here, we investigated such genetic constraints to adaptation in the invasive brown anole (Anolis sagrei)—a tropical ectotherm that was introduced to the southeastern United States, a region with a much colder climate than in its native Caribbean range. We examined thermal physiology for 30 invasive populations and tested for a climatic cline in cold tolerance. Also, we used genomics to identify mechanisms that may limit adaptation. We found no support for a climatic cline, indicating that thermal tolerance did not shift adaptively. Concomitantly, population genomic results were consistent with the occurrence of recombination cold spots that comprise more than half of the genome and maintain long‐range associations among alleles in invasive populations. These genomic regions overlap with both candidate thermal tolerance loci that we identified using a standard genome‐wide association test. Moreover, we found that recombination cold spots do not have a large contribution to population differentiation in the invasive range, contrary to observations in the native range. We suggest that limited recombination is constraining the contribution of large swaths of the genome to adaptation in invasive brown anoles. Our study provides an example of evolutionary stasis during invasion and highlights the possibility that reduced recombination occasionally slows down adaptation in invasive populations.

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  8. Abstract

    Rapid technological improvements are democratizing access to high quality, chromosome-scale genome assemblies. No longer the domain of only the most highly studied model organisms, now non-traditional and emerging model species can be genome-enabled using a combination of sequencing technologies and assembly software. Consequently, old ideas built on sparse sampling across the tree of life have recently been amended in the face of genomic data drawn from a growing number of high-quality reference genomes. Arguably the most valuable are those long-studied species for which much is already known about their biology; what many term emerging model species. Here, we report a highly complete chromosome-scale genome assembly for the brown anole,Anolis sagrei– a lizard species widely studied across a variety of disciplines and for which a high-quality reference genome was long overdue. This assembly exceeds the vast majority of existing reptile and snake genomes in contiguity (N50 = 253.6 Mb) and annotation completeness. Through the analysis of this genome and population resequence data, we examine the history of repetitive element accumulation, identify the X chromosome, and propose a hypothesis for the evolutionary history of fusions between autosomes and the X that led to the sex chromosomes ofA. sagrei.

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  9. Since the invention of electric lighting, artificial light at night (ALAN) has become a defining, and evolutionary novel, feature of human-altered environments especially in cities. ALAN imposes negative impacts on many organisms, including disrupting endocrine function, metabolism, and reproduction. However, we do not know how generalized these impacts are across taxa that exploit urban environments. We exposed brown anole lizards, an abundant and invasive urban exploiter, to relevant levels of ALAN in the laboratory and assessed effects on growth and reproduction at the start of the breeding season. Male and female anoles exposed to ALAN increased growth and did not suffer increased levels of corticosterone. ALAN exposure induced earlier egg-laying, likely by mimicking a longer photoperiod, and increased reproductive output without reducing offspring quality. These increases in growth and reproduction should increase fitness. Anoles, and potentially other taxa, may be resistant to some negative effects of ALAN and able to take advantage of the novel niche space ALAN creates. ALAN and both its negative and positive impacts may play a crucial role in determining which species invade and exploit urban environments. 
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  10. Hybridization is among the evolutionary mechanisms most frequently hypothesized to drive the success of invasive species, in part because hybrids are common in invasive populations. One explanation for this pattern is that biological invasions coincide with a change in selection pressures that limit hybridization in the native range. To investigate this possibility, we studied the introduction of the brown anole (Anolis sagrei) in the southeastern United States. We find that native populations are highly genetically structured. In contrast, all invasive populations show evidence of hybridization among native-range lineages. Temporal sampling in the invasive range spanning 15 y showed that invasive genetic structure has stabilized, indicating that large-scale contemporary gene flow is limited among invasive populations and that hybrid ancestry is maintained. Additionally, our results are consistent with hybrid persistence in invasive populations resulting from changes in natural selection that occurred during invasion. Specifically, we identify a large-effect X chromosome locus associated with variation in limb length, a well-known adaptive trait in anoles, and show that this locus is often under selection in the native range, but rarely so in the invasive range. Moreover, we find that the effect size of alleles at this locus on limb length is much reduced in hybrids among divergent lineages, consistent with epistatic interactions. Thus, in the native range, epistasis manifested in hybrids can strengthen extrinsic postmating isolation. Together, our findings show how a change in natural selection can contribute to an increase in hybridization in invasive populations.

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