Evaluating the effect of overharvesting on genetic diversity and genetic population structure of the coconut crab

Ryman, N., Utter, F. & Laikre, L. Protection of intraspecific biodiversity of exploited fishes. Rev. Fish Biol. Fisheries. 5, 417–446 (1995).

Google Scholar 

Allendorf, F. W., England, P. R., Luikart, G., Ritchie, P. A. & Ryman, N. Genetic effects of harvest on wild animal populations. Trends Ecol. Evol. 23, 327–337 (2008).

PubMed  Google Scholar 

Pinsky, M. L. & Palumbi, S. R. Meta-analysis reveals lower genetic diversity in overfished populations. Mol. Ecol. 23, 29–39 (2014).

PubMed  Google Scholar 

Smith, P. J. Genetic diversity of marine fisheries resources: possible impacts of fishing. FAO Fisheries Technical Paper 344, 1–53 (1994).

CAS  Google Scholar 

Jorgensen, C. et al. Ecology-Managing evolving fish stocks. Science 318, 1247–1248 (2007).

CAS  PubMed  Google Scholar 

Chapman, J. R., Nakagawa, S., Coltman, D. W., Slate, J. & Sheldon, B. C. A quantitative review of heterozygosity–fitness correlations in animal populations. Mol. Ecol. 18, 2746–2765 (2009).

CAS  PubMed  Google Scholar 

Szulkin, M. & David, P. Negative heterozygosity–fitness correlations observed with microsatellites located in functional areas of the genome. Mol. Ecol. 20, 3949–3952 (2011).

PubMed  Google Scholar 

Danzmann, R. G., Ferguson, M. M. & Allendorf, F. W. Heterozygosity and oxygen-consumption rate as predictors of growth and developmental rate in rainbow trout. Physiol. Zool. 60, 211–220 (1987).

Google Scholar 

Thelen, G. C. & Allendorf, F. W. Heterozygosity-fitness correlations in rainbow trout: effects of allozyme loci or associative overdominance? Evolution 55, 1180–1187 (2001).

CAS  PubMed  Google Scholar 

Pujolar, J. M., Maes, G. E., Vancoillie, C. & Volckaert, F. A. M. Growth rate correlates to individual heterozygosity in the European eel. Anguilla anguilla L. Evolution 59, 189–199 (2005).

CAS  PubMed  Google Scholar 

Fassatoui, C., Chenuil, A. & Romdhane, M. S. Relationships between heterozygosity, growth parameters and age in the common pandora Pagellus erythrinus (Sparidae) in the Gabes Gulf (Tunisia). Mar. Ecol. Prog. Ser. 445, 251–261 (2012).

ADS  Google Scholar 

Guinand, B. et al. Genetic structure and heterozygosity–fitness correlation in young-of-the-year sole (Solea solea L.) inhabiting three contaminated West-European estuaries. J. Sea Res. 80, 35–49 (2013).

ADS  Google Scholar 

Zouros, E., Singh, S. M. & Miles, H. E. Growth rate in oysters: an overdominant phenotype and its possible explanations. Evolution 34, 856–867 (1980).

CAS  PubMed  Google Scholar 

Koehn, R. K. & Gaffney, P. M. Genetic heterozygosity and growth rate in Mytilus edulis. Mar. Biol. 82, 1–7 (1984).

Google Scholar 

Bierne, N., Beuzart, I., Vonau, V., Bonhomme, F. & Bédier, E. Microsatellite-associated heterosis in hatchery-propagated stocks of the shrimp Penaeus stylirostris. Aquaculture 184, 203–219 (2000).

Google Scholar 

Coltman, D. W., Bowen, W. D. & Wright, J. M. Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proc. R. Soc. Lond. B Biol. Sci. 265, 803–809 (1998).

CAS  Google Scholar 

Coulson, T. N. et al. Microsatellites reveal heterosis in red deer. Proc. R. Soc. Lond. B Biol. Sci. 265, 489–495 (1998).

CAS  Google Scholar 

Coltman, D. W., Pilkington, J. G., Smith, J. A. & Pemberton, J. M. Parasite-mediated selection against inbred soay sheep in a free-living island population. Evolution 53, 1259–1267 (1999).

PubMed  Google Scholar 

Slate, J. & Pemberton, J. M. Comparing molecular measures for detecting inbreeding depression. J. Evol. Biol. 15, 20–31 (2002).

Google Scholar 

Ledig, F. T., Guries, R. P. & Bonefeld, B. A. The relation of growth to heterozygosity in pitch pine. Evolution 37, 1227–1238 (1983).

Jackson, J. B. et al. Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–637 (2001).

CAS  Google Scholar 

Blueweiss, L. et al. Relationships between body size and some life history parameters. Oecologia 37, 257–272 (1978).

ADS  CAS  PubMed  Google Scholar 

Anderson, M. Sexual Selection. (Princeton University Press,1994).

Jormalainen, V. Precopulatory mate guarding in crustaceans: male competitive strategy and intersexual conflict. Q. REV. Biol. 73, 275–304 (1998).

Google Scholar 

Sato, T., Ashidate, M., Jinbo, T. & Goshima, S. Variation of sperm allocation with male size and recovery rate of sperm numbers in spiny king crab Paralithodes brevipes. Mar. Ecol. Prog. Ser. 312, 189–199 (2006).

ADS  Google Scholar 

Sato, T. & Goshima, S. Impacts of male-only fishing and sperm limitation in manipulated populations of an unfished crab, Hapalogaster dentata. Mar. Ecol. Prog. Ser. 313, 193–204 (2006).

ADS  Google Scholar 

Moland, E., Moland, O. E. & Stenseth, N. C, Maternal influences on offspring size variation and viability in wild European lobster Homarus gammarus. Mar. Ecol. Prog. Ser. 400, 165–173 (2010).

ADS  Google Scholar 

Sato, T., Hamano, K., Sugaya, T. & Dan, S. Effects of maternal influences and timing of spawning on intraspecific variations in larval qualities of the Kuruma prawn Marsupenaeus japonicus. Mar. Biol. 164, 70 (2017).

Google Scholar 

Drew, M. M., Harzsch, S., Stensmyr, M., Erland, S. & Hansson, B. S. A review of the biology and ecology of the robber crab, Birgus latro (Linnaeus, 1767) (Anomura: Coenobitidae). Zool. Anz. 249, 45–67 (2010).

Google Scholar 

Laidre, M. E. Coconut crabs. Curr. Biol. 28, 58–60 (2018).

Google Scholar 

Laidre, M. E. Ruler of the atoll: the world’s largest land invertebrate. Front. Ecol. Environ. 15, 527–528 (2017).

Google Scholar 

Amesbury, S. S. Biological studies on the coconut crab (Birgus latro) in the Mariana Islands. (Agricultural Experiment Station, College of Agriculture and Life Sciences, University of Guam, 1980).

Brown, I. W., & Fielder, D. R. Project overview and literature survey in The Coconut Crab: Aspects of Birgus latro Biology and Ecology in Vanuatu, ACIAR Monograph 8 (eds. Brown, I.W. & Fielder, D. R.) 1–11 (Australian Centre for International Agricultural Research, 1991).

Fletcher, W. J. Coconut crabs in Nearshore Marine Resources of the South Pacific (eds. Wright, A. & Hill, L.) 643–681 (Institute of Pacific Studies, University of the South Pacific, 1993).

Eldredge, L. G. Birgus latro. IUCN Red List of Threatened Species (1996). Available at: http://www.iucnredlist.org/details/2811/0. (Accessed 9 January 2019).

Ministry of the Environment, Government of Japan. The 4th Version of the Red Data Book (2018). Website https://ikilog.biodic.go.jp/Rdb/booklist (accessed 27 February 2019) (in Japanese).

Fujita, Y. Yashigani to hitobito no kurashi. Cancer 19, 41–51 (2010). in Japanese.

Google Scholar 

Sato, T. & Yoseda, K. Influence of size-and sex-biased harvesting on reproduction of the coconut crab Birgus latro. Mar. Ecol. Prog. Ser. 402, 171–178 (2010).

ADS  Google Scholar 

Sato, T. Impacts of large male-selective harvesting on reproduction: illustration with large decapod crustacean resources. Aqua-BioSci. Monogr. 5, 67–102 (2012).

CAS  Google Scholar 

Sato, T., Yoseda, K., Abe, O. & Shibuno, T. Male maturity, number of sperm, and spermatophore size relationships in the coconut crab Birgus latro on Hatoma Island, southern Japan. J. Crust. Biol. 28, 663–668 (2008).

Google Scholar 

Sato, T. Plausible causes for sperm-store variations in the coconut crab Birgus latro under large male-selective harvesting. Aquat. Biol. 13, 11–19 (2011).

Google Scholar 

Sato, T., Yoseda, K., Okuzawa, K. & Suzuki, N. Sperm limitation: possible impacts of large male-selective harvesting on reproduction of the coconut crab Birgus latro. Aquat. Biol. 10, 23–32 (2010).

CAS  Google Scholar 

Sato, T. & Yoseda, K. Reproductive season and female maturity size of coconut crab Birgus latro in Hatoma Island, southern part of Japan. Fish. Sci. 74, 1277–1282 (2008).

CAS  Google Scholar 

Sato, T. & Suzuki, N. Female size as a determinant of larval size, weight, and survival period in the coconut crab, Birgus latro. J. Crust. Biol. 30, 624–628 (2010).

Google Scholar 

Suyama, Y. & Matsuki, Y. MIG-seq: an effective PCR-based method for genome-wide single-nucleotide polymorphism genotyping using the next-generation sequencing platform. Sci. Rep. 5, 16963 nature.com/articles/srep16963 (2015).

ADS  CAS  PubMed  PubMed Central  Google Scholar 

Wachi, N., Matsubayashi, K. W. & Maeto, K. Application of next-generation sequencing to the study of non-model insects. Entomol. Sci. 21, 3–11 (2018).

Google Scholar 

Fletcher, W. J., Brown, I. W. & Fielder, D. R. Moulting and growth characteristics in The Coconut Crab: Aspects of Birgus latro Biology and Ecology in Vanuatu, ACIAR Monograph 8 (eds. Brown, I.W. & Fielder, D. R.) 35–60 (Australian Centre for International Agricultural Research, 1991).

Drew, M. M., Smith, M. J. & Hansson, B. S. Factors influencing growth of giant terrestrial robber crab Birgus latro (Anomura: Coenobitidae) on Christmas Island. Aquat. Biol. 19, 129–141 (2013).

Google Scholar 

Sato, T. et al. Growth of the coconut crab Birgus latro estimated from mark-recapture using passive integrated transponder (PIT) tags. Aquat. Biol. 19, 143–152 (2013).

Google Scholar 

Swartz, W., Sala, E., Tracey, S., Watson, R. & Pauly, D. The spatial expansion and ecological footprint of fisheries (1950 to present). PloS One 5(12), e15143, https://doi.org/10.1371/journal.pone.0015143 (2010).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

McCauley, D. J. et al. Marine defaunation: animal loss in the global ocean. Science 347, 1255641 (2015).

PubMed  Google Scholar 

Cloern, J. E. et al. Human activities and climate variability drive fast-paced change across the world’s estuarine–coastal ecosystems. Global Change Biol. 22, 513–529 (2016).

ADS  Google Scholar 

Hamasaki, K., Sugizaki, M., Dan, S. & Kitada, S. Effect of temperature on survival and developmental period of coconut crab (Birgus latro) larvae reared in the laboratory. Aquaculture 292, 259–263 (2009).

Google Scholar 

Hamasaki, K., Kato, S., Murakami, Y., Dan, S. & Kitada, S. Larval growth, development and duration in terrestrial hermit crabs. Sex. Early Dev. Aquat. Org. 1, 93–107 (2015).

Google Scholar 

Hamasaki, K., Sugizaki, M., Sugimoto, A., Murakami, Y. & Kitada, S. Emigration behaviour during sea-to-land transition of the coconut crab Birgus latro: effects of gastropod shells, substrata, shelters and humidity. J. Exp. Mar. Biol. Ecol. 403, 81–89 (2011).

Google Scholar 

Hamasaki, K., Ishiyama, N. & Kitada, S. Settlement behavior and substrate preference of the coconut crab Birgus latro megalopae on natural substrata in the laboratory. J. Exp. Mar. Biol. Ecol. 468, 21–28 (2015).

Google Scholar 

Nishikawa, A. & Sakai, K. Settlement-competency period of planulae and genetic differentiation of the scleractinian coral Acropora digitifera. Zool. Sci. 22, 391–399 (2005).

PubMed  Google Scholar 

Nakajima, Y., Nishikawa, A., Iguchi, A. & Sakai, K. Gene flow and genetic diversity of a broadcast-spawning coral in northern peripheral populations. PLoS One 5, e11149, https://doi.org/10.1371/journal.pone.0011149 (2010).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

Weese, D. A., Fujita, Y., Hidaka, M. & Santos, S. R. The long and short of it: Genetic variation and population structure of the anchialine atyid shrimp Caridina rubella on Miyako-Jima, Japan. J. Crust. Biol. 32, 109–117 (2012).

Google Scholar 

Lavery, S., Moritz, C. & Fielder, D. R. Changing patterns of population structure and gene flow at different spatial scales in Birgus latro (the coconut crab). Heredity 74, 531 (1995).

CAS  Google Scholar 

Lavery, S., Moritz, C. & Fielder, D. R. Indo-Pacific population structure and evolutionary history of the coconut crab Birgus latro. Mol. Ecol. 5, 557–570 (1996).

Google Scholar 

Hamasaki, K. et al. Genetic diversity and demographic history of the terrestrial hermit crabs Birgus latro and Coenobita brevimanus in the north-western Pacific region. J. Crust. Biol. 35, 793–803 (2015).

Google Scholar 

R core team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria (2016).

Okinawa Prefecture. Riyou kankei siryou. (2017). Website https://www.pref.okinawa.jp/site/kikaku/chiikirito/ritoshinko/h28ritoukankeisiryou.html (accessed 5 December 2019) (in Japanese).

Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnology 3, 294–299 (1994).

CAS  Google Scholar 

Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. journal 1, 10–12 (2011). embnetjournal/article/view/200.

Google Scholar 

Catchen, J. M., Amores, A., Hohenlohe, P., Cresko, W. & Postlethwait, J. H. Stacks: building and genotyping loci de novo from short-read sequences. G3. 1, 171–182 (2011).

CAS  PubMed  Google Scholar 

Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A. & Cresko, W. A. Stacks: an analysis tool set for population genomics. Mol. Ecol. 22, 3124–3140 (2013).

PubMed  PubMed Central  Google Scholar 

Foll, M. & Gaggiotti, O. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180, 977–993 (2008).

Paradis, E. pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics 26, 419–420 (2010).

CAS  PubMed  Google Scholar 

Excoffier, L. & Lischer, H. E. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Res. 10, 564–567 (2010).

Google Scholar 

Peakall, P. E. & Smouse, R. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28, 2537–2539 (2012).

CAS  PubMed  PubMed Central  Google Scholar 

Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Royal Stat. Soc. B 57, 289–300 (1995).

MathSciNet  MATH  Google Scholar 

Coulon, A. GENHET: an easy-to-use R function to estimate individual heterozygosity. Mol. Ecol. Res. 10, 167–169 (2010).

CAS  Google Scholar 

Sundqvist, L., Keenan, K., Zackrisson, M., Prodöhl, P. & Kleinhans, D. Directional genetic differentiation and relative migration. Ecol. Evol. 6, 3461–3475 (2016).

PubMed  PubMed Central  Google Scholar