Multiple paternity and extra-group fertilizations in a natural population of California grunion (Leuresthes tenuis), a beach-spawning marine fish
Although individuals in many fish species move to shallow waters to spawn, the California grunion (Leuresthes tenuis) is almost unique in its constitutive display of synchronous full-emergence beach spawning. During a spawning event, fish ride large waves onshore to spawn on beach land, where their eggs incubate terrestrially. Here, we employ molecular markers to ascertain how this unusual reproductive behavior impacts genetic parentage. We developed and utilized four highly polymorphic microsatellite markers to assess maternal and paternal contributions in a total of 682 progeny from 17 nests of a natural population of L. tenuis. Alleles deduced to be of paternal origin in progeny were used to determine the minimum number of sires per nest and to estimate the true number of sires per nest via Bayesian analysis. We document the following: (a) no instances of multiple maternity for progeny within a nest; (b) a high frequency of nests (88%) with multiple paternity; and (c) an appreciable fraction of nests (18%) in which the estimated number of genetic sires (as many as nine) proved to be greater than the observed number of male attendants, thus implicating occasional extra-group fertilization events. From these and other observations, we also conclude that spawning behavior in grunions may involve site choice but not explicit mate choice. In addition to providing the first analysis of molecular parentage in a beach-spawning fish, we compare our findings to those reported previously for a beach-spawning arthropod, and we discuss the forces that may be maintaining this peculiar reproductive behavior.
KeywordsBeach Mate Choice Mating Behavior Sperm Competition Horseshoe Crab
This work was supported by the National Science Foundation (NSF Grant DGE-0638751) and the University of California, Irvine. Animals were collected with permission from the California Department of Fish and Game granted to R.J.B. with Scientific Collecting Permit ID Number SC-008834. We thank Felipe Barreto and Molly Burke for field assistance, and Felipe Barreto, Vimoksalehi Lukoschek, Andrey Tatarenkov, and two anonymous reviewers for thoughtful comments on the manuscript.
This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.
- Avise JC (2004) Molecular markers, natural history, and evolution, 2nd edn. Sinauer Associates, Sunderland, MSGoogle Scholar
- Avise JC, Jones AG, Walker D, DeWoody JA et al (2002) Genetic mating systems and reproductive natural histories of fishes: lessons for ecology and evolution. Annu Rev Genet 36:19–45. doi: https://doi.org/10.1146/annurev.genet.36.030602.090831 CrossRefGoogle Scholar
- Breder CM Jr, Rosen DE (1966) Modes of reproduction in fishes. Natural History Press, Garden City, NYGoogle Scholar
- Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5:453–455. doi: https://doi.org/10.1111/j.1365-294X.1996.tb00336.x CrossRefGoogle Scholar
- Clark FN (1925) The life history of Leuresthes tenuis, an atherine fish with tide controlled spawning habits. Calif Dep Fish Game Fish Bull 10:1–51Google Scholar
- Halliday TR (1983) The study of mate choice. In: Bateson P (ed) Mate choice. Cambridge University Press, Cambridge, pp 3–32Google Scholar
- Hancock JM (1999) Microsatellites and other simple sequences: genomic context and mutational mechanisms. In: Goldstein DB, Schlötterer C (eds) Microsatellites: evolution and applications. Oxford University Press, New York, pp 1–9Google Scholar
- Hoelzel AR, Green A (1998) PCR protocols and population analysis by direct DNA sequencing and PCR-based DNA fingerprinting. In: Hoelzel AR (ed) Molecular genetic analysis of populations: a practical approach, 2nd edn. Oxford University Press, New York, pp 201–235Google Scholar
- Middaugh DP, Kohl HW, Burnett LE (1983) Concurrent measurement of intertidal environmental variables and embryo survival for the California grunion, Leuresthes tenuis, and Atlantic silverside, Menidia menidia (Pisces: Atherinidae). Calif Fish Game 69:89–96Google Scholar
- Miller DJ, Lea RN (1972) Guide to the coastal marine fishes of California. Calif Depart Fish Game Fish Bull 157:1–235Google Scholar
- Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev Camb Philos Soc 45:525–567. doi: https://doi.org/10.1111/j.1469-185X.1970.tb01176.x CrossRefGoogle Scholar
- Pemberton JM, Slate J, Bancroft DR, Barrett JA (1995) Nonamplifying alleles at microsatellite loci: a caution for parentage and population studies. Mol Ecol 4:249–252. doi: https://doi.org/10.1111/j.1365-294X.1995.tb00214.x CrossRefGoogle Scholar
- Smyder EA, Martin KLM (2002) Temperature effects on egg survival and hatching during the extended incubation period of California grunion, Leuresthes tenuis. Copeia 2002:313–320. doi: https://doi.org/10.1643/0045-8511(2002)002[0313:TEOESA]2.0.CO;2 CrossRefGoogle Scholar
- Thompson WF, Thompson JB (1919) The spawning of the grunion (Leuresthes tenuis). Calif Depart Fish Game Fish Bull 3:1–29Google Scholar
- Walker BW (1949) Periodicity of spawning by the Grunion, Louresthes tenuis, an Atherine Fish. PhD thesis, University of California, Los AngelesGoogle Scholar
- Walker BW (1952) A guide to the grunion. Calif Fish Game 38:409–420Google Scholar
Open AccessThis is an open access article distributed under the terms of the Creative Commons Attribution Noncommercial License (https://creativecommons.org/licenses/by-nc/2.0), which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.