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Does Energy Availability Predict Gastropod Reproductive Strategies?
Craig R.McClain National Evolutionary Synthesis Center, Duke University
McClain et al. Proceedings of the Royal Society B, in press
Two female bubble-rafting violet snails, Janthina exigua. Egg capsules are attached to the underside of the floats.
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Life requires energy
Veined Octopus (Amphioctopus marginatus) eating a crab
Three distinct types of energy !affect biological
systems
1. solar radiation in the form of photons!
2. thermal kinetic energy as indexed by temperature!
3.chemical potential energy stored in reduced carbon compounds
Clarke & Gaston (2006) Proc Roy Soc B
Planktotrophic: feed in the plankton during their larval stage and are considered to have longer dispersal potential
Lecithotrophic: larvae derive nourishment from yolk and are non-feeding and are considered to have longer dispersal potential
Direct: young develop directly into the adult form without a larval phase and typically have limited dispersal potential
Thermal kinetic energy and chemical potential energy are posited to influence reproductive strategies
Low Temp Food
% P
lank
toni
c La
rvae
slow larval growth long larval duration
fast larval growth short larval duration
Predation
High Temp Food
Thorson
Thermal kinetic energy and chemical potential energy are posited to influence reproductive strategies
Low Food
% P
lank
toni
c La
rvae
planktonic larvae cheap minimize larval/adult competition
dispersal phases allow for bet hedging
direct development expensive retention of larvae favored
High Food
Hermaphroditic nudibranchs, Siphopteron sp. nov., from the Great Barrier Reef !!
R. Lange, J. Werminghausen and N. Anthes. Cephalo-traumatic secretion transfer in a hermaphrodite sea slug. Proceedings of the Royal Society B. Published online November 13, 2013. doi: 10.1098/rspb.2013.2424.!!J.M. Koene et al. A syringe-like love dart injects male accessory gland products in a tropical hermaphrodite. PLOS ONE. Vol. 8, July 2013, p.e69968. doi:10.1371/journal.pone.00e69968
Thermal kinetic energy and chemical potential energy are posited to influence reproductive strategies
Low Food
% H
erm
aphr
oditi
sm
density low mate availability low
density high mate availability high
High Food
Abundance
For 189 !gastropod families !collected data on!!larval development !(dispersing v. not)!!& hermaphroditism !(present v. absent)
Analyses• Binary and binomial regression models were implemented in R using the package
MCMCglmm
• uninformative priors and uniformly low levels of belief
• Model chains were run for 500,000 iterations with a burn-in of 200,000 iterations and thinning intervals of 100 iterations.
• To evaluate convergence, we assessed the mixing of Markov chain Monte Carlo (MCMC) chains
• Chemical energy available to the gastropods was estimated as particulate organic carbon (POC) flux (g of C m−2 year−1) based on the Lutz et al. (2007) model.
• Temperature data was gathered from the NODC database (Locarnini et al. 2010).
• For each family, we quantified the median and standard deviation of carbon flux and temperature over their known latitudinal and depth ranges.
• Taxonomic Order—from the most current taxonomy for Gastropoda (Bouchet & Rocroi 2005)—was included as a random effect to account for the possible effects of shared phylogenetic history in our model. A more explicit estimation of phylogenetic covariance was not possible due to the current lack of a comprehensive molecular phylogeny for this clade.
sqrt (Median Carbon Flux)
Probability o
f O
ccurrence
Mixed
Direct
Lecithotrophic
Planktotrophic
50 150 2500.0
0.5
1.0
the odds of having planktotrophic larvae versus direct development
decreasing by 1% with every one-unit increase in the square root of
carbon flux
Opposite of that predicted by Thorson
50 150 2500.0
0.5
1.0
sqrt (Median Carbon Flux)
Probability o
f O
ccurrence
Hermaphroditic
Non-Hermaphroditic
Result opposite of prediction!!
Relationship disappears when accounting for taxonomic
relatedness.
0.0 0.5 1.0 1.5 2.0
Caenogastropoda
Cocculiniformia
Eupulmonata
Heterobranchia
Neritimorpha
Patellogastropoda
Vetigastropoda
Log Median POC flux(g of C m-2 year-1)
Distribution
Basal metabolic rates of nudibranchs are highest among gastropods.!!Metabolically expensive to be a simultaneous hermaphrodite
Planktotrophic larvae increases!
Direct development decreases!
with decreasing productivity. !
Thus, low energy availability is selecting for adaptations for energy conservation or bet heeding in a patchy environment.!
!
The result for hermaphroditism is opposite of prediction, !
decreases not increases with decreasing energy availability !
and likely related to shifts in metabolic demand not life reproductive strategy
Does Energy Availability Predict Gastropod Reproductive Strategies?
Acknowledgments
Coauthors: Ryan Filler (Duke University) and Josh Auld (West Chester University) !Statistical Guidance: Carlos Botero (NC State University) !Funding: National Evolutionary Synthesis Center (NSF Grant #EF-0905606)
National Evolutionary Synthesis Center