Chaotic genetic patchiness without sweepstakes reproduction in the shore crab Hemigrapsus oregonensis

Vol. 548: 139–152, 2016 doi: 10.3354/meps11628 MARINE ECOLOGY PROGRESS SERIES Mar Ecol Prog Ser Published April 21 O PEN A CCESS Chaotic genetic patchiness without sweepstakes reproduction in the shore crab Hemigrapsus oregonensis Brendan H. Cornwell 1, 3, *, Jennifer L. Fisher 2 , Steven G. Morgan 2 , Joseph E. Neigel 1 Department of Biology, University of Louisiana at Lafayette, PO Box 42451, Lafayette, Louisiana 70504, USA Bodega Marine Laboratory, University of California at Davis, PO Box 247, Bodega Bay, California 94923, USA Present address: Center for Population Biology, University of California at Davis, Davis, California 95616, USA ABSTRACT: Fine-scale spatial and temporal variation in the genetic composition of benthic recruits, known as chaotic genetic patchiness, is often observed in marine and estuarine species with planktonic larvae. Several explanations have been proposed for chaotic genetic patchiness, including sweepstakes reproductive success, variability in larval source, and natural selection. In a survey of the green shore crab Hemigrapsus oregonensis in Bodega Bay, California, USA, allele frequencies at a mitochondrial single nucleotide polymorphism were found to differ significantly among samples of first-stage zoeae and between zoeae and adults. Sweepstakes reproductive success is unlikely to be responsible because the fecundity of this species is too low and there was no reduction in genetic diversity among zoeae. In principle, influxes of larvae from genetically dis- tinct populations over 500 km to the north could have caused these differences; however, coales- cent estimates indicated that gene flow from these distant populations has been very low and it is unlikely that first-stage zoeae would have been transported such great distances. The possibility remains that natural selection, directly or indirectly, is responsible for the observed patchiness in mitochondrial allele frequencies. KEY WORDS: Mitochondrial DNA · Single nucleotide polymorphism · Natural selection · Phylogeography INTRODUCTION In the 1990s, the hypothesis of sweepstakes repro- ductive success (SRS) was promoted to explain tem- poral changes in allozyme frequencies in populations of oysters and other marine species with high fecun- dity and planktonic larvae (Hedgecock 1994). SRS requires individual fecundity to be so high that it is possible for just a few individuals, the lucky ‘sweep- stakes winners,’ to spawn the majority of a genera- tion’s progeny (Hedrick 2005). Such extreme vari- ance in reproductive success would result in genetic drift strong enough to create substantial temporal changes in allele frequencies (reviewed by Hedge- cock & Pudovkin 2011). *Corresponding author: bhcornwell@ucdavis.edu Another phenomenon cited as evidence of SRS is ‘chaotic genetic patchiness’ (CGP), whereby small differences in allele frequencies occur among cohorts of settling larvae. The concept of CGP was intro- duced by Johnson & Black (1982) to describe the fine-scale spatial heterogeneity in allozyme frequen- cies they observed in an intertidal limpet. They found that patches of recruits that were settling at different times differed in allozyme frequencies because the genetic composition of the larval pool changed over time (Johnson & Black 1984). They also concluded that the genetic changes in the larval pool were caused by natural selection because those changes were larger than could be explained by geographic variation in larval sources. Since then, SRS, rather © The authors 2016. Open Access under Creative Commons by Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com