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Shortest Recorded Vertebrate Lifespan Found in a Coral Reef Fish

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Shortest Recorded Vertebrate Lifespan Found in a Coral Reef Fish CORE Metadata, citation and similar papers at core.ac.uk Provided by Elsevier - Publisher Connector Current Biology Vol 15 No 8 R288 monkeyflowers and other taxa are just 35 days, of which at least 10 helping to overcome this gap. Correspondence are taken to reach sexual maturity The ‘bottom up’ or genetic (Figure 1B). This provides the approach to studying speciation species with a remarkable three- has hunted down genes Shortest recorded week window in which to responsible for premating and reproduce and contribute to the postmating isolation, and then vertebrate next generation. shown that the gene sequences lifespan found in a Already constrained by time, the exhibit signatures of recent lifetime fecundity of E. sigillata is selection. But this approach has coral reef fish further restricted by small adult told us little about the nature of body sizes of 11–20 mm, limiting that selection. Is selection the number of eggs a female can divergent or has divergence Martial Depczynski and produce. Yet pygmy gobies are an occurred under uniform selection? David R. Bellwood incredibly successful group, Was selection in response to numbering some 70 species with environmental differences? Was it Extreme short lifespans are of a geographic distribution natural or sexual selection? interest because they mark encompassing reefs across the Finally, we still know little about current evolutionary boundaries Indian and Pacific Oceans [1]. To how mate preferences evolve and biological limits within which investigate lifetime fecundity, we within and between populations life’s essential tasks must be bred pygmy gobies in captivity. during the process of speciation. successfully accomplished. Here Females were able to spawn Sexual selection by mate choice we document the remarkable successive clutches of 108–163 might be a near-universal process eight week lifespan of the coral eggs (egg size 0.75 x 0.55 mm) in speciation, but what drives the reef pygmy goby Eviota sigillata within an 11–17 day period, divergence of mate preferences to [1] (Figure 1A): the shortest suggesting that females have the begin with? recorded lifespan for any potential to produce just three Speciation study is in the midst vertebrate. Coral reef pygmy clutches in a lifetime — a little of a surge of research effort, and gobies spend their first three over 400 eggs. Given that larval part of the reason is that answers weeks as larvae in the open ocean mortality in reef fishes typically to many of these questions before undergoing metamorphosis exceeds 95% [3], high larval appear at last to be within reach. and returning to settle on the reef, survivorship is critical for this We expect that a combination of where they mature within 1–2 species, and males fan and guard phenotypic and genetic weeks and have a maximum adult their eggs until hatching, a approaches will soon close the lifespan of just three and a half reproductive strategy that greatly gap between the genes and the weeks. enhances offspring survivorship mechanisms of selection, and The rapid transition from larvae [4]. With an average generation yield a fuller account of how most to settlement and then maturity is time of just 49 days, E. sigillata species in nature have formed. recorded in the calcareous may produce up to 7.4 ‘earstones’ (otoliths) of fishes by generations per year. Further reading the deposition of periodic For small species living in Coyne, J.A., and Orr, H.A. (2004). Speciation, (Sunderland, MA: concentric rings; these provide not ecological settings where high Sinauer). only a sensitive record of time but extrinsic mortality rates exist, Orr, H.A., Masly, J.P., and Presgraves, a chronological ‘black box’ which evolution often favors a ‘live fast, D.C. (2004). Speciation genes. Curr. imprints the age at which die young’ stratagem where rapid Opin. Genet. Dev. 14, 675–679. Panhuis, T.M., Butlin, R., Zuk, M., and important events take place [2]. growth and maturation are favored Tregenza, T. (2001). Sexual Each day, pygmy gobies lay down [5,6], presumably as compensation selection and speciation. Trends a new ring in their otoliths, much for reduced life expectancy. For Ecol. Evol. 16, 364–371. as a tree does for each year. We example, the vertebrate that Rieseberg, L.H. (1997). Hybrid origins of plant species. Annu. Rev. Ecol. collected 319 E. sigillata previously had the shortest Syst. 28, 359–389. specimens from the Great Barrier recorded lifespan and for which Schluter, D. (2000). The Ecology of Reef over both summer and winter ageing data are available — the Adaptive Radiation, (Oxford: periods. Age was determined after Turquoise killifish, Notobranchius Oxford University Press). Servedio, M.R., and Noor, M.A.F. validation of daily otolith ring furzeri — inhabits seasonal rain (2003). The role of reinforcement in deposition, and sexual maturity pools in equatorial Africa and must speciation: theory and data. Annu. status identified using histological complete its reproductive cycle Rev. Ecol. Evol. Syst. 34, 339–364. techniques. A settlement ‘check’ before these pools disappear [7]. Turelli, M., Barton, N.H., and Coyne, J.A. (2001). Theory and speciation. mark in the otolith at 23–27 days Under laboratory conditions N. Trends Ecol. Evol. 16, 330–343. marked the transition from open furzeri survives for only 12 weeks. ocean larvae to settlement on the Interestingly, recorded extremes in Zoology Department and Biodiversity reef. Analyses of the largest vertebrate life history traits, such Research Centre, University of British individuals showed that E. sigillata as the smallest [8] and earliest Columbia, Vancouver, British Columbia, Canada, V6T 1Z4. has a maximum total lifespan of 59 maturing [9] vertebrates, are also E-mail: [email protected], days, with a maximum post- found in coral reef fish species. [email protected] settlement lifespan on the reef of Despite the prevalence of such life Magazine R289 Figure 1. A vertebrate with Supplemental data A the shortest recorded Supplemental data showing lifespan. methodology, detailed results and (A) The cryptic coral reef additional references are available at pygmy goby (Eviota sigillata) http://www.current-biology.com/ in its natural reef habitat cgi/content/full/15/8/R288/DC1/ (photo J. E. Randall). (B) Size at age in E. sigillata (n = 50). Pygmy gobies live complex References lives divided into an open 1. Jewett, S.L. and Lachner, E.A. ocean pelagic larval phase (1983). Seven new species of the (~24 days) followed by Indo-Pacific genus Eviota (Pisces: Gobiidae). Proc. Biol. Soc. Wash. settlement onto reefs, sexual B 20 96, 780-806. Pelagic larval Coral reef maturation (day 34–38) and 18 phase phase 2. Pannella, G. (1971). Fish otoliths: death within 59 days. Daily growth layers and periodical 16 patterns. Science 173, 1124-1127. 14 3. Sale, P.F. (1991). The Ecology of Fishes on Coral Reefs. (London: 12 Academic Press). 10 4. Neff, B.D. (2003). Decisions about parental care in response to 8 Reef settlement Reef perceived paternity. Nature 422, Total length (mm) length Total 6 716-719. Female maturation 5. Gadgil, M., and Bossert, W.H. 4 (1970). Life historical consequences 2 Male maturation of natural selection. Am. Nat. 104, 1-24. 0 6. Reznick, D.N. and Endler, J.A. 0 5 10 15 20 25 30 35 40 45 50 55 60 Age in days (1982). The impact of predation on Current Biology life history evolution in Trinidadian guppies (Poecilia reticulate). Evol. 36, 160-177. history extremes in coral reef [10] that are small enough 7. Valdesalici, S. and Cellerino, A. (2003). Extremely short lifespan in fishes, no-one has questioned why (<10 cm) to remain at high risk of the annual fish Notobranchius coral reefs support such biological predation throughout their lives. furzeri. Proc. R. Soc. Lond. B extremes. Whether a result of high predation (Suppl.) 270, S189-S191. Are the ecological conditions rates, environmental stability, 8. Watson, H. and Walker Jr., H.J. (2004). The world’s smallest that support the evolution of constant habitat availability, or vertebrate, Schindleria brevipinguis, extremes in life history designs simply a consequence of their a new paedomorphic species in the particularly strong in coral reef exceptional biodiversity, coral family Schindleriidae (Perciformes: ecosystems? To investigate the reefs appear to provide the Gobioidei), Rec. Aust. Mus. 56, 139- 142. link between extreme life history ecological conditions that support 9. Kon, T. and Yoshino, T. (2002). traits and levels of mortality in the evolution and maintenance of Extremely early maturity found in coral reef environments we extremes in vertebrate life history. the Okinawan gobioid fishes. conducted an experimental field Completing all the necessary Ichthyol. Res. 49, 224-228. 10. Ackerman, J.L., and Bellwood, D.R. study on small coral reef fish demands of life within eight weeks (2000). Reef fish assemblages: a re- communities on the Great Barrier is a considerable evolutionary evaluation using enclosed rotenone Reef. We tagged 146 small reef achievement for a vertebrate. By stations. Mar. Ecol. Prog. Ser. 206, fishes from a range of species, accelerating life’s key events, E. 227-237. including 36 E. sigillata, at 12 sites, sigillata stands as a living Centre for Coral Reef Biodiversity, and returned 9 days later to example of the extreme Department of Marine Biology, James recapture the survivors. Daily adaptability of the vertebrate life Cook University, Townsville, Queensland mortality rates averaging 7.8% cycle and highlights the potential 4811, Australia. (± 2.7% sd) indicate the severe for coral reef ecosystems to biological time constraints and reveal further extremes in The editors of Current Biology intense selective pressure vertebrate biology. welcome correspondence on imposed on these small coral reef fishes. Acknowledgements any article in the journal, but We thank G. Allen, J. H. Choat, A.
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