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Habitat-based isolating barriers are not strong in the speciation of ecologically divergent squirrels (Tamiasciurus douglasii and T. hudsonicus)

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Abstract

Adaptations to different environments between closely related species can be important drivers of reproductive isolation during speciation due to either habitat isolation between species or reduced fitness in hybrids that possess suboptimal adaptations. Hybrid zones are useful natural arenas to explore how ecologically divergent species compete for habitat in sympatry and how possible differences in their habitat use may contribute to the speciation process. We investigated habitat selection by sister species of tree squirrels, the Douglas squirrel and the red squirrel, that have evolved in different forest types in allopatry and hybridize in a transitional forest. We first used genome-wide SNP data and admixture analyses to classify individuals into parental or hybrid classes. Next, we estimated home ranges with radio telemetry data and then used a novel ground-based lidar system to measure forest canopy structure of squirrel home ranges, midden sites, and marginally used forest habitat. We found hybrids consisting of multiple hybrid classes were intermixed with both parental species in the same forest with varying canopy structure complexity. On average, Douglas squirrels utilized forests with slightly greater structural complexity than either red squirrels or hybrids, while marginally used forests were the least structurally complex. Interestingly, hybrid squirrels were not relegated to marginal habitat and were successful in mating among each other and with both parental species. As such, our study suggests that prezygotic-ecological isolation and postzygotic-hybrid infertility, and postzygotic ecological inviability of hybrids are not strong barriers in the speciation process between Douglas squirrels and red squirrels.

Significance statement

Closely related species that become geographically divided often encounter different environments and thus evolve different adaptations. Sometimes, these species meet again and produce hybrids. Hybrids often have lower fitness due to their inferior adaptations. We studied a pair of closely related squirrels that evolved in different environments and meet and produce hybrids in a secondary contact zone. Despite these species evolving in allopatry in very different forest types, they do not select different forest characteristics while in sympatry in the hybrid zone. Furthermore, hybrids do not show major differences in types of habitats that they choose and are capable of defending territories and reproducing among each other and with both parental species. In summary, prezygotic and postzygotic isolating mechanisms associated with habitat selection do not appear to have an important role in promoting species divergence.

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Acknowledgments

We are grateful to S. Doyle, A. Esposto, G. Heyer, N. Israel, D. Kirchmeier, and S. Malinich for field assistance. We thank two anonymous reviewers for useful suggestions on the manuscript. The genomic sequencing was carried by the DNA Technologies and Expression Analysis Cores at the UC Davis Genome Center, supported by NIH Shared Instrumentation Grant 1S10OD010786-01.

Data accessibility

Analyses reported in this article can be reproduced using the data provided by Fotis et al. (2019).

Funding

This research was supported by the startup fund from The Ohio State University for Andreas Chavez.

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Authors and Affiliations

  1. USDA Forest Service, Northern Research Station, 359 Main Road, Delaware, OH, 43015, USA

    Alexander T. Fotis

  2. Department of Evolution, Ecology, and Organismal Biology, The Ohio State University, 318 W. 12th Avenue, Columbus, OH, 43210, USA

    Sahil Patel & Andreas S. Chavez

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  1. Alexander T. Fotis
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  2. Sahil Patel
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  3. Andreas S. Chavez
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Contributions

ATF and ASC contributed to the conceptualization and study design. ATF performed the LiDAR data collection and ecological analyses and SP conducted the genomic data collection. ASC conducted the home range and admixture analyses. ATF and ASC contributed to the writing and revising of the manuscript.

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Correspondence to Andreas S. Chavez.

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Ethical approval

All animal handling techniques were approved by The Ohio State University’s IACUC (protocol #2017A00000031) and adhered to the American Society of Mammalogists guidelines for the use of wild mammals in research (Sikes & The Animal Care and Use Committee of the American Society of Mammalogists 2016).

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The authors declare that they have no conflict of interest.

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Communicated by A. I Schulte-Hostedde

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Fotis, A.T., Patel, S. & Chavez, A.S. Habitat-based isolating barriers are not strong in the speciation of ecologically divergent squirrels (Tamiasciurus douglasii and T. hudsonicus). Behav Ecol Sociobiol 74, 32 (2020). https://doi.org/10.1007/s00265-020-2814-5

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