Award Abstract # 1459384
Collaborative Research: The impacts of mating system variation on ecological performance and evolutionary diversification in a clade of marine snails

NSF Org: OCE
Division Of Ocean Sciences
Recipient: UNIVERSITY OF NORTH CAROLINA AT WILMINGTON
Initial Amendment Date: March 18, 2015
Latest Amendment Date: March 18, 2015
Award Number: 1459384
Award Instrument: Standard Grant
Program Manager: Daniel J. Thornhill
OCE
 Division Of Ocean Sciences
GEO
 Directorate for Geosciences
Start Date: May 1, 2015
End Date: April 30, 2021 (Estimated)
Total Intended Award Amount: $368,247.00
Total Awarded Amount to Date: $368,247.00
Funds Obligated to Date: FY 2015 = $368,247.00
History of Investigator:
  • Stephanie Kamel (Principal Investigator)
    kamels@uncw.edu
Recipient Sponsored Research Office: University of North Carolina at Wilmington
601 S COLLEGE RD
WILMINGTON
NC  US  28403-3201
(910)962-3167
Sponsor Congressional District: 07
Primary Place of Performance: University of North Carolina at Wilmington
601 South College Rd
Wilmington
NC  US  28403-3201
Primary Place of Performance
Congressional District:
07
Unique Entity Identifier (UEI): L1GPHS96MUE1
Parent UEI:
NSF Program(s): BIOLOGICAL OCEANOGRAPHY,
EVOLUTIONARY ECOLOGY
Primary Program Source: 01001516DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1174, 8214, 9117
Program Element Code(s): 165000, 737700
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.050

ABSTRACT

At present, virtually nothing is known about how mating systems vary within and among individuals, populations, and species of marine organisms. Indeed, characterizing mating system variation in the sea, and its effects on fundamental ecological and evolutionary patterns and processes, now represents a challenge perhaps equal in importance to the study of population connectivity that has occupied many marine ecologists for the last three decades. Snails in the genus Nucella are important intertidal predators and provide an exceptional model system for exploring how mating systems control critical ecological and evolutionary processes and patterns. By integrating insights from population and behavioral ecology, and life-history theory, combined with genetic, experimental, and phylogenetic approaches, this project will generate novel insights into the impacts of mating system variation on the ecological and evolutionary dynamics of marine systems. This project will significantly advance our understanding of how mating system variation in marine systems influences individuals, populations, and species, with important implications for better predicting how processes such as climate change, habitat fragmentation, and harvesting will influence population dynamics, speciation, and ecosystem function. Through partnerships with established programs, including (1) a UC Davis-Howard University program that supports research internships at UC Davis for Howard undergraduates every year; (2) new programs at Bodega Marine Lab (CAMEOS and ISOpods) to develop self-contained marine science modules in the classroom; (3) training of K-12 educators through the Sacramento Area Science Project; (4) a newly funded NSF grant at UC Davis to produce a new, statewide ?Modeling scientific practice in high school biology? curriculum; (5) military veteran placements through the UNCW Office of Transitional programs; and (6) the UNCW eTEAL (Experiencing Transformative Education through Applied Learning) program, emphasizing undergraduate research in molecular ecology, this project will train numerous under-represented students, scientists, and teachers in modern ecology, genetics, and phylogenetics. In addition, the project interfaces with multiple educational programs through partnerships with the Exploratorium, NOAA?s expansion of west coast marine sanctuaries and outreach programs, and science communications programs at UC Davis and UNCW. NSF funding over the last 4 years has supported 5 Ph.D. students (4 women), 3 postdocs (1 woman, 1 Hispanic), and 9 undergraduates (5 women, 2 minority).

Worldwide, anthropogenic and natural processes are rapidly modifying patterns of environmental variation that affect the traits of individuals, populations, species, and communities, and that ultimately threaten both biodiversity and ecosystem functioning. These threats are often viewed in the context of (a) reductions in population size or density; (b) changes in demographic and genetic connectivity; and (c) Allee effects, where reduced local densities limit mating success. Though less-well studied ? especially in marine systems ? environmental perturbations can also rapidly alter the mating systems of populations. Numerous studies show that intra- and inter-specific variation in mating systems has major impacts on a broad spectrum of ecological and evolutionary processes (e.g., dispersal, population dynamics, life-history diversity, and speciation), that can profoundly influence the sustainability of marine ecosystems. The investigators? previous NSF-funded work established, for the first time in any marine organism, that the mating system strongly influences both offspring size variation and reproductive compatibilities in the predatory marine snail Nucella ostrina. This work raised several major questions regarding the ecology of marine organisms. Through field experiments, mating trials, genetic analyses, and phylogenetically explicit comparisons, the present project will comprehensively examine the fundamental roles that mating systems play in (1) generating ecologically relevant trait variation; (2) driving reproductive isolation; and (3) shaping macro-ecological patterns of life-history variation. This research will broaden our understanding of the critical role that mating systems play in the ecology and diversification of marine organisms, and provide the foundation for understanding how changes in population demographics and mating systems can influence both short term population dynamics and longer term responses to environmental change.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Shamblott, K.M., Reneker, J.L. and S.J. Kamel "The thermal impacts of beach nourishment across a regionally important loggerhead sea turtle (Caretta caretta) rookery" Ecosphere , 2021
Adrian, A.J., Lack, C.E., and Kamel, S.J. "Kin aggregations occur in eastern oyster Crassostrea virginica reefs despite limited regional genetic differentiation" Marine Ecology Progress Series , v.584 , 2017
Jaymie L. Reneker & Stephanie J. Kamel "The Maternal Legacy: Female Identity Predicts Offspring Sex Ratio in the Loggerhead Sea Turtle" Scientific Reports , v.6 , 2016 10.1038/srep29237
Kamel, S.J., and Williams, P.D. "Relatedness and resource exploitation: implications for within-brood size variation" Oikos , v.126 , 2017
PD Williams, SJ Kamel. "Evolutionary invasion analysis in structured populations." Evolutionary Biology , 2021

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

Worldwide, anthropogenic and natural processes are rapidly modifying patterns of environmental variation. Though less-well studied – especially in marine systems - environmental perturbations can also rapidly alter the mating systems of populations. The present project proposed to examine the roles that mating systems play in generating ecologically relevant trait variation and driving reproductive isolation in a marine snail. Mating systems vary widely among populations of snails and can be an important driver of variation in offspring size. How then do these differences influence offspring survival? Field based mark-recapture studies did not find significant differences in size among surviving snails at sites that varied widely in predation pressure, even though snails have a well-known size refugium with respect to crab predators. Several potential compensatory mechanisms emerged, such as aperture width: snails can reduce their aperture opening to decrease mortality when exposed to high densities of predators. However, as with shell size, aperture width was not a strong determinant of survival, though geographic variation in the strength of this relationship was apparent. 

 

Aperture width was significantly correlated with an individual’s behavioral response (i.e. personality). Snails with wider apertures displayed shy behavioral types and showed limited behavioral plasticity as compared to snails with narrower apertures, indicating that snails at higher risk of predation behaviorally compensate by displaying consistent predator avoidance behaviors. In addition to decreased plasticity, they also displayed higher predictability in their behavior, with lower residual variance around the reaction norm than snails with narrower apertures. Like size, individual behavioral responses varied geographically. 

 

Increasing evidence indicates that the expression of personality is contingent upon social context; group dynamics may thus be key in determining how individuals interact. When single snails were exposed to a predator, neither size nor personality influenced survival. However, in experimental predation trials, groups of shy individuals had the lowest survival, while groups of bold individuals had the highest. While mean mortality in bold snails remained unchanged across treatments, mortality in the mixed groups was strongly dependent on the presence of bold individuals. Indeed, the presence of a few bold individuals emerged as especially effective in decreasing mortality in the shy individuals. The influence of personality on survival is conditional on group personality composition, indicating that social context can greatly impact the success of its individual members. 

 

Additionally, parasite infection modified several aspects of behavior, leading to important changes in the interaction with predators. Infection status and size influenced behavioral plasticity: when individuals were uninfected, larger snails became bolder in high-risk environments while smaller snails became shier. This pattern was reversed in infected individuals: smaller snails became significantly bolder in high-risk environments and larger snails became shier. Infected individuals showed higher responsiveness overall, suggesting that infection status can, in certain cases, significantly impact an individual’s response to environmental changes. 

 

A growing number of studies on marine organisms is showing that the density, genetic composition, and trait distribution of groups of interacting conspecifics can exert strong effects on many aspects of performance. These effects of social context, often mediated by mating system variation, should be especially important in sessile or sedentary benthic marine communities, where intraspecific competition for food and space is generally intense, and mating often occurs between neighbors. By integrating insights from behavioral ecology and life-history theory, combined with genetic, field, and experimental approaches, this project generated novel insights into the role of mating system variation on the ecological and evolutionary dynamics of marine systems. This proposal has supported doctoral, masters and undergraduate students, and has provided training opportunities and applied learning experiences to military veterans, women, and students from historically underrepresented groups with a specific focus on the collection and analysis of data in molecular and evolutionary ecology. 


Last Modified: 03/21/2022
Modified by: Stephanie Kamel

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