Scott A. Taylor

Speciation in marine taxa is dynamic and complex, often occurring in the absence of absolute geographic barriers to gene flow. Boobies comprise a clade of seven highly mobile seabird species with high diversity in the eastern Pacific Ocean, where no land barriers separate extant sister species and hybridization is widespread. They exhibit striking diversity in bare-part coloration, an important signal of mate quality, and possess a novel multiple sex chromosome system (Z ₁ Z ₂ Z ₁ Z ₂ / Z ₁ Z ₂ W), likely resulting from a fusion between an ancestral autosomal microchromosome and the W chromosome. To understand speciation processes in the context of gene flow, we sequenced and analyzed 29 short-read booby genomes and assembled a reference northern gannet genome to (1) test for introgression, (2) characterize genomic patterns of divergence across species, and (3) investigate the gene content and evolution of the neo-sex chromosome. We found that divergence among eastern Pacific sister taxa is temporally associated with periods of glacial maxima. Between periods of glacial maxima, two pairs of sister species (blue-footed and Peruvian boobies; masked and Nazca boobies) exhibit strong signatures of episodic introgression, indicating that speciation has occurred over multiple periods of divergence followed by gene flow. However, in the third pair of sister species, genomic signatures showed higher divergence within brown booby populations than between brown and Cocos boobies. We also identified the epidermal differentiation complex – a gene cassette involved in skin, feather, beak, and claw development – on the neo-sex region of the W chromosome, where it spans the boundary between the putatively recombining and non-recombining regions, with interspecific variation in the exact recombination suppression boundary. We inferred that this complex may contribute to diversity in feather and bare part coloration across boobies. Together, these results reveal that diversification and speciation in a clade of highly mobile seabirds emerged from a complex evolutionary history involving historical climate dynamics, introgression, and sex chromosome evolution.

Rates of hybridization are increasing globally, but we lack an understanding of both the history and evolutionary outcomes of hybridization for most species. This makes it difficult to understand whether, and to what extent, humans are influencing hybridization. Integrating field studies with whole genome data is a critical next step for understanding hybridization and the extent of human influences on evolution. Here, we combine 3 years of population monitoring with 569 whole genomes to characterize the reproductive ecology of, and hybridization between, two common songbirds, black-capped (Poecile atricapillus) and mountain (P. gambeli) chickadees, for which hybridization is correlated with human habitat disturbance across North America. Working within a geographic region that we previously identified as a hotspot of contemporary chickadee hybridization we find that, despite geographic and temporal breeding overlap, few early generation hybrids are produced indicating that reproductive barriers typically prevent contemporary hybridization. Yet, every chickadee we sampled in sympatry possessed heterospecific ancestry, indicating that both contemporary and historical hybridization have occurred during the evolutionary history of chickadees in Colorado. Why contemporary hybridization continues to occur despite evidence for character displacement of chickadee song remains less clear, but urban forests may play a role.

There is a tremendous amount of intra- and inter-specific variation in animal cognitive abilities, and understanding the evolutionary mechanisms generating such variation is an important issue in evolutionary biology. Here we review our research on spatial cognition in food-caching chickadees, which use spatial cognitive abilities to recover previously made food caches to survive harsh winters. This work ranges from comparing multiple populations along environmental gradients to investigating the causes and consequences of individual variation in spatial learning and memory abilities, to describing the genetic basis of such variation. Our data show that (i) chickadees in harsher environments have better spatial cognitive abilities and a larger hippocampus with more hippocampal neurons, with differences between populations persisting in common garden experiments; (ii) chickadees tested in the wild show extensive individual variation in their learning and memory abilities; (iii) this variation is highly heritable and has a genetic basis; and (iv) this variation is associated with significant differences in survival, lifespan and reproductive success. Overall, our data provide strong evidence that spatial cognitive abilities in food-caching chickadees are shaped by natural selection, which generates differences among populations living across heterogeneous environmental conditions. This article is part of the Theo Murphy meeting issue ‘Selection shapes diverse animal minds’.

Determining the genetic architecture of traits involved in adaptation and speciation is one of the key components of understanding the evolutionary mechanisms behind biological diversification. Hybrid zones provide a unique opportunity to use genetic admixture to identify traits and loci contributing to partial reproductive barriers between taxa. Many studies have focused on the temporal dynamics of hybrid zones, but geographical variation in hybrid zones that span distinct ecological contexts has received less attention. We address this knowledge gap by analyzing hybridization and introgression between black-capped and Carolina chickadees in two geographically remote transects across their extensive hybrid zone, one located in eastern and one in central North America. Previous studies demonstrated that this hybrid zone is moving northward as a result of climate change but is staying consistently narrow due to selection against hybrids. In addition, the hybrid zone is moving ~5× slower in central North America compared to more eastern regions, reflecting continent-wide variation in the rate of climate change. We use whole genome sequencing of 259 individuals to assess whether variation in the rate of hybrid zone movement is reflected in patterns of hybridization and introgression, and which genes and genomic regions show consistently restricted introgression in distinct ecological contexts. Our results highlight substantial similarities between geographically remote transects and reveal large Z-linked chromosomal rearrangements that generate measurable differences in the degree of gene flow between transects. We further use simulations and analyses of climatic data to examine potential factors contributing to continental-scale nuances in selection pressures. We discuss our findings in the context of speciation mechanisms and the importance of sex chromosome inversions in chickadees and other species.

Cryptic genetic differentiation is being increasingly documented in birds and other organisms using genome‐wide variation. A recent example of cryptic genetic differentiation in a widespread species with conserved morphology is the northern house wren Troglodytes aedon . We found that, despite extremely similar morphology and no documented vocal differences, the two subspecies of the northern house wren, T. a. aedon (eastern) and T. a. parkmanii (western), exhibited both nuclear and mitochondrial genomic differentiation. Individuals present along the Front Range of the Colorado Rocky Mountains possessed nuclear genetic variation intermediate between T. a. aedon and T. a. parkmanii ; additionally, both divergent mitochondrial lineages, corresponding to the western and eastern northern house wren populations, occur in Colorado. However, the dynamics of this putative contact zone (i.e. amount of hybridization or introgression) and the degree of differentiation between the two subspecies remain uncharacterized. To expand our understanding of northern house wren population genetic differentiation and explore the possibility of hybridization, we used a double digest restriction‐site associated (ddRAD) approach and sequenced 127 northern house wrens, including 109 individuals from across Colorado and Wyoming, as well as nine individuals each from eastern and western allopatric regions. Our results highlight that T. a. aedon occur significantly further west than previously thought, and provide evidence for weak population structure within the northern house wren, while generally setting the stage for future investigations of northern house wren population genomics and the genetic basis of cryptic speciation.

Character displacement theory predicts that closely-related co-occurring species should diverge in relevant traits to reduce costly interspecific interactions such as competition or hybridization. While many studies document character shifts in sympatry, few provide corresponding evidence that these shifts are driven by the costs of co-occurrence. Black-capped (Poecile atricapillus) and mountain chickadees (P. gambeli) are closely-related, ecologically similar, and broadly distributed songbirds with both allopatric and sympatric populations. In sympatry, both species appear to suffer costs of their co-occurrence: 1) both species are in worse body condition compared to allopatry and 2) hybridization sometimes yields sterile offspring. Here, we explored character displacement in the songs of black-capped and mountain chickadees by characterizing variation in male songs from sympatric and allopatric populations. We found that mountain chickadees sing differently in sympatry versus allopatry. Specifically, they produced more notes per song, were more likely to include an extra introductory note, and produced a smaller glissando in their first notes compared to all other populations. Combined with previous research on social dominance and maladaptive hybridization between black-capped and mountain chickadees, we posit that differences in sympatric mountain chickadee song are population-wide shifts to reduce aggression from dominant black-capped chickadees and/or prevent maladaptive hybridization.

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.

In hybrid zones, whether barrier loci experience selection mostly independently or as a unit depends on the ratio of selection to recombination as captured by the coupling coefficient. Theory predicts a sharper transition between an uncoupled and coupled system when more loci affect hybrid fitness. However, the extent of coupling in hybrid zones has rarely been quantified. Here, we use simulations to characterize the relationship between the coupling coefficient and variance in clines across genetic loci. We then reanalyze 25 hybrid zone data sets and find that cline variances and estimated coupling coefficients form a smooth continuum from high variance and weak coupling to low variance and strong coupling. Our results are consistent with low rates of hybridization and a strong genome-wide barrier to gene flow when the coupling coefficient is much greater than 1, but also suggest that this boundary might be approached gradually and at a near constant rate over time.

Haemosporidian parasite communities are broadly similar in Boulder County, Colorado, between two common songbirds –– the Black-capped Chickadee (Poecile atricapillus) and Mountain Chickadee (Poecile gambeli). However, Mountain Chickadees appear more likely to be infected with Plasmodium, and potentially experience higher infection burdens with Leucocytozoon in contrast to Black-capped Chickadees. We found that elevation change (and associated ecology) drives the distributions of these parasite genera. For Boulder County chickadees, environmental factors play a more important role in structuring haemosporidian communities than host evolutionary differences. However, evolutionary differences are likely key to shaping the probability of infection, infection burden, and whether an infection remains detectable over time. We found that for recaptured birds, their infection status (i.e., presence or absence of detectable parasite infection) tends to remain consistent across capture periods. We sampled 234 chickadees between 2017 and 2021 across a ~1,500-m elevation gradient from low elevation (i.e., the city of Boulder) to comparatively high elevation (i.e., the CU Boulder Mountain Research Station). It is unknown whether long-term haemosporidian abundance trends have changed over time in our sampling region. However, we ask whether potentially disparate patterns of Plasmodium susceptibility and Leucocytozoon infection burden could be playing a role in the negative population trends of Mountain Chickadees.