Plasticity in parental effects confers rapid larval thermal tolerance in the estuarine anemone Nematostella vectensis

Author:

Rivera Hanny E.123ORCID,Chen Cheng-Yi4,Gibson Matthew C.45ORCID,Tarrant Ann M.2ORCID

Affiliation:

1. Massachusetts Institute of Technology-Woods Hole Oceanographic Institution (MIT-WHOI) Joint Program in Oceanography/Applied Ocean Science and Engineering, Cambridge and Woods Hole, MA, USA

2. Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA

3. Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 64110, USA

4. Stowers Institute for Medical Research, Kansas City, MO, USA

5. Department of Anatomy and Cell Biology, The University of Kansas School of Medicine, Kansas City, KS 66160, USA

Abstract

ABSTRACT Parental effects can prepare offspring for different environments and facilitate survival across generations. We exposed parental populations of the estuarine anemone, Nematostella vectensis, from Massachusetts to elevated temperatures and quantified larval mortality across a temperature gradient. We found that parental exposure to elevated temperatures resulted in a consistent increase in larval thermal tolerance, as measured by the temperature at which 50% of larvae die (LT50), with a mean increase in LT50 of 0.3°C. Larvae from subsequent spawns returned to baseline thermal thresholds when parents were returned to normal temperatures, indicating plasticity in these parental effects. Histological analyses of gametogenesis in females suggested that these dynamic shifts in larval thermal tolerance may be facilitated by maternal effects in non-overlapping gametic cohorts. We also compared larvae from North Carolina (a genetically distinct population with higher baseline thermal tolerance) and Massachusetts parents, and observed that larvae from heat-exposed Massachusetts parents had thermal thresholds comparable to those of larvae from unexposed North Carolina parents. North Carolina parents also increased larval thermal tolerance under the same high-temperature regime, suggesting that plasticity in parental effects is an inherent trait for N. vectensis. Overall, we find that larval thermal tolerance in N. vectensis shows a strong genetic basis and can be modulated by parental effects. Further understanding of the mechanisms behind these shifts can elucidate the fate of thermally sensitive ectotherms in a rapidly changing thermal environment.

Funder

Betty and Gordon Moore Foundation

National Defense Science and Engineering Graduate fellowship

Gates Millennium Scholars Program

Martin Family Fellowship for Sustainability

American Association of University Women

Stowers Institute for Medical Research

Publisher

The Company of Biologists

Subject

Insect Science,Molecular Biology,Animal Science and Zoology,Aquatic Science,Physiology,Ecology, Evolution, Behavior and Systematics

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