Something Darwin didn't know about barnacles: spermcast mating in a common stalked species

Most free-living barnacles are hermaphroditic, and eggs are presumed to be fertilized either by pseudo-copulation or self-fertilization. Although the common northeast Pacific intertidal gooseneck barnacle, Pollicipes polymerus, is believed only to cross-fertilize, some isolated individuals well outside penis range nonetheless bear fertilized eggs. They must therefore either self-fertilize or—contrary to all prior expectations about barnacle mating—obtain sperm from the water. To test these alternative hypotheses, we collected isolated individuals bearing egg masses, as well as isolated pairs where at least one parent carried egg masses. Using 16 single nucleotide polymorphism markers, we confirmed that a high percentage of eggs were fertilized with sperm captured from the water. Sperm capture occurred in 100 per cent of isolated individuals and, remarkably, even in 24 per cent of individuals that had an adjacent partner. Replicate subsamples of individual egg masses confirmed that eggs fertilized by captured sperm occurred throughout the egg mass. Sperm capture may therefore be a common supplement to pseudo-copulation in this species. These observations (i) overturn over a century of beliefs about what barnacles can (or cannot) do in terms of sperm transfer, (ii) raise doubts about prior claims of self-fertilization in barnacles, (iii) raise interesting questions about the capacity for sperm capture in other species (particularly those with short penises), and (iv) show, we believe for the first time, that spermcast mating can occur in an aquatic arthropod.

[1]  D. Desai,et al.  Reproduction in Balanus amphitrite Darwin (Cirripedia: Thoracica): influence of temperature and food concentration , 2006 .

[2]  Settlement and recruitment patterns of a pedunculate barnacle, Pollicipes polymerus Sowerby, off La Jolla, California , 1989 .

[3]  D. Anderson,et al.  Sperm Ultrastructure in the Cirripedia and its Phylogenetic Significance , 1990 .

[4]  M. Hart,et al.  Spawning, copulation and inbreeding coefficients in marine invertebrates , 2005, Biology Letters.

[5]  E. Charnov The theory of sex allocation. , 1984, Monographs in population biology.

[6]  Á. Carracedo,et al.  Multiplex SNaPshot for detection of BRCA1/2 common mutations in Spanish and Spanish related breast/ovarian cancer families , 2007, BMC Medical Genetics.

[7]  Sérgio L. S. Bueno,et al.  INFESTATION BY OCTOLASMIS LOWEI (CIRRIPEDIA: POECILASMATIDAE) IN CALLINECTES DANAE AND CALLINECTES ORNATUS (DECAPODA: PORTUNIDAE) FROM SÃO SEBASTIÃO, BRAZIL , 2002 .

[8]  J. Hoch,et al.  An Individual Barnacle, Semibalanus balanoides, with Two Penises , 2009 .

[9]  Matthew Z. Anderson,et al.  Barnacles: Structure, function, development and evolution , 1993 .

[10]  A. J. Pemberton,et al.  The third way: spermcast mating in sessile marine invertebrates. , 2006, Integrative and comparative biology.

[11]  M. F. Strathmann Reproduction and development of marine invertebrates of the northern Pacific coast , 1987 .

[12]  Eric S. Lander,et al.  Large-scale discovery and genotyping of single-nucleotide polymorphisms in the mouse , 2000, Nature Genetics.

[13]  H. Barnes,et al.  Further Observations on Self‐Fertilization in Chthamalus Sp. , 1958 .

[14]  A. R. Palmer,et al.  Precisely proportioned: intertidal barnacles alter penis form to suit coastal wave action , 2008, Proceedings of the Royal Society B: Biological Sciences.

[15]  T. Kajihara,et al.  Breeding and moulting of barnacles under rearing conditions , 1991 .

[16]  C. Darwin The balanidæ, (or sessile cirripedes); the verrucidæ, etc., etc., etc. , 1968 .

[17]  C. A. Lewis Development of the gooseneck barnacle Pollicipes polymerus (Cirripedia: Lepadomorpha): Fertilization through settlement , 1975 .

[18]  Yoichi Yusa,et al.  Adaptive evolution of sexual systems in pedunculate barnacles , 2012, Proceedings of the Royal Society B: Biological Sciences.

[19]  M. Barnes Pedunculate Cirripedes of the genus Pollicipes , 1996 .

[20]  M. Barnes Egg production in cirripedes , 1989 .

[21]  D. Crisp,et al.  Evidence of self-fertilization in certain species of barnacles , 1956, Journal of the Marine Biological Association of the United Kingdom.

[22]  S Rozen,et al.  Primer3 on the WWW for general users and for biologist programmers. , 2000, Methods in molecular biology.

[23]  A. Palmer,et al.  Precise tuning of barnacle leg length to coastal wave action , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[24]  P. Duchesne,et al.  Stable genetic polymorphism in heterogeneous environments: balance between asymmetrical dispersal and selection in the acorn barnacle , 2006, Journal of evolutionary biology.

[25]  J. Høeg Sex and the single cirripede: a phylogenetic perspective , 1995 .

[26]  C. Patrick Doncaster,et al.  Population consequences of mutual attraction between settling and adult barnacles , 2003 .

[27]  Lars Kaderali,et al.  Primer-design for multiplexed genotyping. , 2003, Nucleic acids research.

[28]  S. Kalinowski,et al.  Individual Identification and Distribution of Genotypic Differences Between Individuals , 2006 .

[29]  R. Grosberg,et al.  Love the one you're with: proximity determines paternity success in the barnacle Tetraclita rubescens , 2012, Molecular ecology.

[30]  M. Barnes The reproductive periods and condition of the penis in several species of common cirripedes , 1992 .

[31]  A. B. Yule,et al.  Self-fertilisation in Balanus improvisus Darwin , 1990 .