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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.
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Spiranthes bightensis (Orchidaceae), a New and Rare Cryptic Hybrid Species Endemic to the U. S. Mid-Atlantic Coast
Recognizing species diversity is challenging in genera that display interspecific similarity and intraspecific variation; hybridization and the evolution of cryptic hybrid species amplifies these challenges. Recent molecular and morphological research focused on the systematics of Spiranthes (Orchidaceae) support hybrid speciation as an important driver of species diversity, particularly within the S. cernua species complex. Working under an integrated history-bound phylogenetic species concept, new molecular and morphometric data provide evidence for a new and rare cryptic hybrid species resulting from the ancient hybridization of S. cernua × S. odorata, here described as S. bightensis. Although S. bightensis is regionally sympatric with S. cernua it does not co-occur with that species, and it is allopatric with respect to S. odorata. Endemic to a narrow region extending from the Delmarva Peninsula to Long Island, New York, this new species occurs in the shadow of the Northeast megalopolis and appears to have undergone a major population decline over the last 200 years. By recognizing this distinct evolutionary lineage as a new species, this research is the first step towards developing conservation protocols for this rare species and highlights the importance of the North American Geologic Coastal Plain for biodiversity conservation and evolution.
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- Award ID(s):
- 1802034
- PAR ID:
- 10257051
- Date Published:
- Journal Name:
- Phytotaxa
- Volume:
- 498
- Issue:
- 3
- ISSN:
- 1179-3155
- Page Range / eLocation ID:
- 159–176
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.11646/phytotaxa.498.3.2
