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