An official website of the United States government
Abstract BackgroundHybridization between evolutionary lineages has profound impacts on the fitness and ecology of hybrid progeny. In extreme cases, the effects of hybridization can transcend ecological timescales by introducing trait novelty upon which evolution can act. Indeed, hybridization can even have macroevolutionary consequences, for example, as a driver of adaptive radiations and evolutionary innovations. Accordingly, hybridization is now recognized as a motor for macrobial evolution. By contrast, there has been substantially less progress made towards understanding the positive eco-evolutionary consequences of hybridization on holobionts. Rather, the emerging paradigm in holobiont literature is that hybridization disrupts symbiosis between a host lineage and its microbiome, leaving hybrids at a fitness deficit. These conclusions, however, have been drawn based on results from predominantly low-fitness hybrid organisms. Studying “dead-end” hybrids all but guarantees finding that hybridization is detrimental. This is the pitfall that Dobzhansky fell into over 80 years ago when he used hybrid sterility and inviability to conclude that hybridization hinders evolution. Goldschmidt, however, argued that rare saltational successes—so-called hopeful monsters—disproportionately drive positive evolutionary outcomes. Goldschmidt’s view is now becoming a widely accepted explanation for the prevalence of historical hybridization in extant macrobial lineages. Aligning holobiont research with this broader evolutionary perspective requires recognizing the importance of similar patterns in host–microbiome systems. That is, rare and successful “hopeful holobionts” (i.e., hopeful monsters at the holobiont scale) might be disproportionately responsible for holobiont evolution. If true, then it is these successful systems that we should be studying to assess impacts of hybridization on the macroevolutionary trajectories of host–microbiome symbioses. ResultsIn this paper, we explore the effects of hybridization on the gut (cloacal) and skin microbiota in an ecologically successful hybrid lizard,Aspidoscelis neomexicanus. Specifically, we test the hypothesis that hybrid lizards have host-associated (HA) microbiota traits strongly differentiated from their progenitor species. Across numerous hybrid microbiota phenotypes, we find widespread evidence of transgressive segregation. Further, microbiota restructuring broadly correlates with niche restructuring during hybridization. This suggests a relationship between HA microbiota traits and ecological success. ConclusionTransgressive segregation of HA microbiota traits is not only limited to hybrids at a fitness deficit but also occurs in ecologically successful hybrids. This suggests that hybridization may be a mechanism for generating novel and potentially beneficial holobiont phenotypes. Supporting such a conclusion, the correlations that we find between hybrid microbiota and the hybrid niche indicate that hybridization might change host microbiota in ways that promote a shift or an expansion in host niche space. If true, hybrid microbiota restructuring may underly ecological release from progenitors. This, in turn, could drive evolutionary diversification. Using our system as an example, we elaborate on the evolutionary implications of host hybridization within the context of holobiont theory and then outline the next steps for understanding the role of hybridization in holobiont research.
more »
« less
This content will become publicly available on February 1, 2027
Sleep disruption as a potential mechanism contributing to post‐zygotic reproductive isolation in hybrids
ABSTRACT Hybridization occurs when different species mate and produce offspring. Although hybridization can have negative consequences for cognitive performance, the mechanisms underlying those effects are still poorly understood. A fundamental physiological process found in all animals studied to date that could be disrupted in hybrids is sleep. Given that mechanisms that occur within the brain during sleep may help maintain optimal cognitive performance, here we outline the potential impacts of hybridization on sleep and cognition. We suggest that sleep loss caused by hybridization could lead to negative impacts for neural and molecular mechanisms (e.g. neurogenesis, synaptic plasticity, and brain gene expression) associated with cognition, which may help explain some of the cognitive deficiency recently observed in hybrid birds. However, we acknowledge that these mechanisms may instead be directly impacted by hybridization, which in turn could also disrupt sleep with similar negative consequences for cognition. Limitations in sleep processes apparent in hybrids might influence hybrid fitness and therefore act as a post‐zygotic isolating barrier.
more »
« less
- Award ID(s):
- 1754909
- PAR ID:
- 10658446
- Publisher / Repository:
- Wiley
- Date Published:
- Journal Name:
- Biological Reviews
- Volume:
- 101
- Issue:
- 1
- ISSN:
- 1464-7931
- Page Range / eLocation ID:
- 297 to 313
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Sleep is critical to a variety of cognitive functions and insufficient sleep can have negative consequences for mood and behavior across the lifespan. An important open question is how sleep duration is related to functional brain organization which may in turn impact cognition. To characterize the functional brain networks related to sleep across youth and young adulthood, we analyzed data from the publicly available Human Connectome Project (HCP) dataset, which includesn‐back task‐based and resting‐state fMRI data from adults aged 22–35 years (taskn = 896; restn = 898). We applied connectome‐based predictive modeling (CPM) to predict participants' mean sleep duration from their functional connectivity patterns. Models trained and tested using 10‐fold cross‐validation predicted self‐reported average sleep duration for the past month fromn‐back task and resting‐state connectivity patterns. We replicated this finding in data from the 2‐year follow‐up study session of the Adolescent Brain Cognitive Development (ABCD) Study, which also includesn‐back task and resting‐state fMRI for adolescents aged 11–12 years (taskn = 786; restn = 1274) as well as Fitbit data reflecting average sleep duration per night over an average duration of 23.97 days. CPMs trained and tested with 10‐fold cross‐validation again predicted sleep duration fromn‐back task and resting‐state functional connectivity patterns. Furthermore, demonstrating that predictive models are robust across independent datasets, CPMs trained on rest data from the HCP sample successfully generalized to predict sleep duration in the ABCD Study sample and vice versa. Thus, common resting‐state functional brain connectivity patterns reflect sleep duration in youth and young adults.more » « less
-
Delmore, Kira (Ed.)Abstract Hybridization produces a range of outcomes from advantageous to disadvantageous, and a goal of genetic research is to understand the gene interactions that generate these outcomes. Interactions between cytoplasmic elements, such as mitochondria, and the nucleus may be particularly vulnerable to accruing disadvantageous combinations as a result of their different rates of evolution. Consequently, mitonuclear incompatibilities may play an important role in hybrid outcomes even if their negative impacts could be masked for some fitness measures by heterosis in first-generation (F1) hybrids. We used Tigriopus californicus, a model system for mitonuclear incompatibilities that is also known for exhibiting heterosis in the F1 generation and outbreeding depression in later generations, to test whether heterosis or outbreeding depression would occur when mitonuclear mismatch was paired with a stress that heavily impacts mitochondrial processes—specifically, hypoxia. We generated 284 parental and 436 F1 hybrids from four population crosses (720 total) and compared parental and F1 populations for hypoxia tolerance. We observed that, on average, F1 hybrids were less likely to survive a hypoxia stress test than parental populations, although we did not detect a statistically significant trend (P = 0.246 to 0.614). This suggests that hypoxia may be a particularly intense stressor for mitonuclear coordination and hybridization outcomes vary by trait.more » « less
-
Demographic responses of hybridizing cinquefoils to changing climate in the Colorado Rocky MountainsAbstract Hybridization between taxa generates new pools of genetic variation that can lead to different environmental responses and demographic trajectories over time than seen in parental lineages. The potential for hybrids to have novel environmental tolerances may be increasingly important in mountainous regions, which are rapidly warming and drying due to climate change. Demographic analysis makes it possible to quantify within‐ and among‐species responses to variation in climate and to predict population growth rates as those conditions change. We estimated vital rates and population growth in 13 natural populations of two cinquefoil taxa (Potentilla hippianaandP. pulcherrima) and their hybrid across elevation gradients in the Southern Rockies. Using three consecutive years of environmental and demographic data, we compared the demographic responses of hybrid and parental taxa to environmental variation across space and time. All three taxa had lower predicted population growth rates under warm, dry conditions. However, the magnitude of these responses varied among taxa and populations. Hybrids had consistently lower predicted population growth rates thanP. hippiana. In contrast, hybrid performance relative toP. pulcherrimavaried with population and climate, with the hybrid maintaining relatively stable growth rates while populations ofP. pulcherrimashrank under warm, dry conditions. Our findings demonstrate that hybrids in this system are neither intrinsically unfit nor universally more vigorous than parents, suggesting that the demographic consequences of hybridization are context‐dependent. Our results also imply that shifts to warmer and drier conditions could have particularly negative repercussions forP. pulcherrima, which is currently the most abundant taxon in the study area, possibly as a legacy of more favorable historical climates. More broadly, the distributions of these long‐lived taxa are lagging behind their demographic trajectories, such that the currently less commonP. hippianacould become the most abundant of thePotentillataxa as this region continues to warm and dry.more » « less
-
Abstract Hybrid zones can be used to identify traits that maintain reproductive isolation and contribute to speciation. Cognitive traits may serve as post-mating reproductive isolating barriers, reducing the fitness of hybrids if, for example, misexpression occurs in hybrids and disrupts important neurological mechanisms. We tested this hypothesis in a hybrid zone between two subspecies of Swainson’s thrushes (Catharus ustulatus) using two cognitive tests—an associative learning spatial test and neophobia test. We included comparisons across the sexes and seasons (spring migration and winter), testing if hybrid females performed worse than males (as per Haldane’s rule) and if birds (regardless of ancestry or sex) performed better during migration, when they are building navigational maps and encountering new environments. We documented reduced cognitive abilities in hybrids, but this result was limited to males and winter. Hybrid females did not perform worse than males in either season. Although season was a significant predictor of performance, contrary to our prediction, all birds learned faster during the winter. The hypothesis that cognitive traits could serve as post-mating isolating barriers is relatively new; this is one of the first tests in a natural hybrid zone and non-food-caching species. We also provide one of the first comparisons of cognitive abilities between seasons. Future neurostructural and neurophysiological work should be used to examine mechanisms underlying our behavioral observations.more » « less
