Host genetic variation and microenvironment shape an emergent plant–antagonist interaction

Abstract

Geographic mosaics of interspecific interactions can arise as a consequence of intrinsic and extrinsic deterministic factors. In this study, we took advantage of the recent discovery of a specialist leaf-miner (Caloptilia triadicae) on invasive Chinese tallow (Triadica sebifera) in the southeastern United States to examine deterministic drivers of variation in plant–animal antagonistic interactions. We conducted a common garden study to assess the influence of intrinsic host genetic variation and extrinsic microenvironment on Triadica traits as well as Caloptilia infestation and mortality. We found that tree size, branch leaf density, and leaf toughness differed according to multilocus estimates of genetic variation. Host genetic variation also influenced mortality of early instar Caloptilia, but had little effect on peak or late season infestation. Triadica from hyperinvasive populations were larger, exhibited reduced leaf density and tougher leaves, and had the lowest levels of peak season Caloptilia infestation, but also had the lowest levels of early instar mortality. Microhabitat variation associated with edge effects influenced tree size as well as late season infestation. These findings indicate that CaloptiliaTriadica interactions reflect seasonal shifts in the relative influence of intrinsic and extrinsic drivers, where peak season interactions largely reflect genetic variation in hosts, and late–season interactions reflect microenvironmental conditions. Further study of Caloptilia infestations could offer additional understanding of novel interactions that arise following species introductions.

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Acknowledgments

We would like to thank E. Siemann, J. Carillo, G. Wheeler, and S. Wright for providing access to necessary resources and the UHCC common garden; E. Siemann, J. Ding, J. K. Davis, J. Karubian, S. Van Bael, A. Kawahara, C. Richards-Zawacki, V.L. and M.L. Aberdeen for support, guidance and input on this study; M.S. Fox, H.L. Handley, A.B. Uzunian, A.B. Quinlan, K.A. Hazen, M. Dakin, B. Kravis, S. Piper, C. Amabile, and R. da Silva Nascimento for field and laboratory assistance. Funding for this study was provided by Tulane University.

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Correspondence to Rebecca F. Hazen.

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Supplementary material 1 Appendix 1. Descriptive statistics. (a) Number of individuals examined for trait and genetic analyses, and population-level genetic variability statistics. As a result of differences in survivorship and growth rate, there were unequal numbers of trees with attainable leaves from each focal population. (b) Indices of genetic diversity per locus (c) Descriptive statistics for dependent variables (JPEG 85 kb)

Supplementary material 2 Appendix 2. Heat map of the edge effect variable. Rows 26-36, at the top of the garden plot, were removed prior to the study and afforded assessment of trees that were on and away from the forest edge. The other edges of the garden perimeter had two to three intact rows of buffer trees and were assigned edge values of three or four accordingly. Other trees within the garden were assigned values relative to their distance from the closest outermost tree (JPEG 95 kb)

Supplementary material 3 Appendix 3. Output of Triadica GLMs testing for potential interactions between genetic variation and response to microenvironment. Genetic variation was characterized according to (left) the first factor of the PCA of multilocus microsatellite variation, and (right) categorical identity according to origin (native, early introduction, later introduction) (JPEG 35 kb)

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Hazen, R.F., Blum, M.J. Host genetic variation and microenvironment shape an emergent plant–antagonist interaction. Evol Ecol 30, 1043–1060 (2016). https://doi.org/10.1007/s10682-016-9868-x

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Keywords

  • Caloptilia triadicae
  • Triadica sebifera
  • Intrinsic deterministic factors
  • Extrinsic deterministic factors
  • Biocontrol
  • Seasonal shift