Life-history and thermal tolerance traits display different thermal plasticities and relationships with temperature in the marine polychaete Ophryotrocha labronica La Greca and Bacci (Dorvilleidae)
Highlights
► The phenotypic plasticity of life history and thermal tolerance is investigated. ► They show respectively a non-monotonic and monotonic trend. ► The thermal history of the individuals influences the life-history patterns. ► Cold tolerance is a more plastic trait than heat tolerance. ► A functional dependence to temperature and no evolutionary trade-offs are observed.
Introduction
For ectotherms, temperature is a major factor in shaping phenotypic variation across environments, due to its direct effect on metabolic rates and impact at all levels of biological organisation, including phenotypically plastic responses (Angiletta, 2009, Cossins and Bowler, 1987, Hochachka and Somero, 2002, Hofmann, 2005, Nylin and Gotthard, 1998). Variation in life-history and physiological traits in response to thermal changes are well-studied examples of phenotypic plasticity (Dhillon and Schulte, 2011, Hollander and Butlin, 2010, Sokolova and Pörtner, 2003, Spicer and Gaston, 1999, Stearns and Koella, 1986), since the ability to adjust the phenotype in response to temperature allows species to successfully colonise and persist in thermally-heterogeneous environments (Agrawal, 2001, Ghalambor et al., 2007). Additionally, physiological plasticity resulting from thermal acclimation allows organisms to adjust their metabolic processes to persist under conditions that would otherwise be disadvantageous or even lethal. Taken together, plasticity in life-history and physiological traits allow an organism to maximise its fitness according to the new set of environmental conditions countering the effects of environmental changes in temperature (DeWitt et al., 1998, Hoffmann, 1995, Pigliucci, 1996, Pigliucci, 2001, Spicer and Gaston, 1999, Stearns, 1992).
The benefits of plasticity are extensively reported in the literature (for review see Angiletta, 2009, Nylin and Gotthard, 1998, Pigliucci, 2001, West-Eberhard, 2003), with acclimation generally assumed to improve function in the environment that induces it by enhancing individual fitness (Beneficial acclimation hypothesis — Bennett and Lenski, 1997, Hochachka and Somero, 2002, Hoffmann and Parsons, 1989, Huey and Berrigan, 1996, Leroi et al., 1994, Levins, 1969, Rome et al., 1992, Scheiner, 1993). Nonetheless, acclimation in one trait can impose costs, and be deleterious for the optimal functioning of other organismal activities (Non-beneficial acclimation hypothesis — Hoffmann, 1995, Huey and Berrigan, 1996; but see Wilson and Franklin, 2002). Surprisingly, factors that constrain plasticity are not as well understood (DeWitt et al., 1998, Lind and Johansson, 2009, Relyea, 2002), although limits to the array of phenotypes that a plastic genotype can express, as well as fitness costs associated with the ability to be plastic, are recognised as the main factors limiting the evolution of phenotypic plasticity itself (DeWitt et al., 1998, Lind and Johansson, 2009). Physiological and life-history performances, in fact, cannot be maximised at any time and in any environment: limitations in resource availability, as well as the occurrence of morphological, physiological and phylogenetic constraints, limit the expression of phenotypic plasticity (Charnov, 1993, Lind and Johansson, 2009, Reznick et al., 2000, Ricklefs, 2000, Ricklefs and Wikelski, 2002, Roff, 1992, Stearns, 1992) in ways that may lead to negative associations, or trade-offs, between traits (Clutton-Brock et al., 1982, Reznick, 1985, Roff, 1992, Rose et al., 1996, Stearns, 1989, Stearns, 1992, Zera and Harschmann, 2001). The assumption that the evolution of traits is restricted or biassed by fitness trade-off is a core component of evolutionary life-history theories, as it provides an explanation for the widespread occurrence of variable life-history traits in natural populations (Reznick et al., 2000, Stearns, 1992).
The strategies evolved by organisms to cope with thermal heterogeneity result from the interaction of a species' physiology and life history, which are themselves constrained by the costs and limits associated with plasticity (Angiletta, 2009). Tolerating changes in environmental temperature requires energy to adjust, maintain and repair physiological systems, and how this energy is redistributed to different functions undoubtedly shapes the survivorship, growth and reproductive performances of an organism (Angiletta, 2009, Stearns, 1992, Zera and Harschmann, 2001). More specifically, since physiological costs are a large component of animal energy budgets (Angilletta, 2001, Lardies and Bozinovic, 2008, Sibly and Calow, 1986), variations in thermal tolerance following an acclimation process may affect life-history traits (e.g. growth and reproduction performances), ultimately affecting organisms' fitness. As a consequence, understanding how a suite of physiological and life-history traits reciprocally respond to temperature is a fundamental issue which needs to be explored if we are to comprehend the evolutionary processes underlying adaptation to thermally fluctuating-environments (Angiletta, 2009, Boher et al., 2010, Stocks and De Block, 2011). This issue may be addressed by analysing thermal tolerance limits, which can be used as a proxy to describe an individual's ability to tolerate and perform physiological functions under different temperatures regimes, and thus help investigate the link between thermal physiology and thermal ecology (Bozinovic et al., 2011, Deutsch et al., 2008, Huey and Stevenson, 1979, Ribeiro et al., 2012).
The marine polychaete Ophryotrocha labronica La Greca and Bacci 1962 (Polychaeta, Dorvilleidae) offers the opportunity to gain insights into the link between organismal fitness, measured as life-history traits, and physiological functions for the first time in a marine ectotherm. O. labronica is a subtidal gonochoristic polychaete broadly distributed along Mediterranean coasts, and it is commonly found in the fouling communities that colonise harbour and lagoon environments (Prevedelli and Simonini, 2003, Simonini et al., 2009, Thornhill et al., 2009). This species experiences high thermal fluctuations, due to the seasonality and unpredictability of temperature in its habitat (Prevedelli et al., 2005, Simonini et al., 2009, Simonini et al., 2010, Thornhill et al., 2009). Water temperatures, in fact, can range on average from 8–9 to 27–28 °C in winter and summer, respectively, reaching extreme temperatures of 4 °C and 30.5 °C recorded during our sampling surveys (Massamba-N'Siala et al., 2011; personal obs.). Laboratory and field experiments have highlighted the strong influence exerted by temperature on many life-history and demographic traits of O. labronica, as well as on its population dynamics (Åkesson, 1976, Prevedelli and Simonini, 2001, Prevedelli et al., 2005). Based on these studies, both a broad thermal tolerance window and a high level of temperature-dependent phenotypic plasticity are expected in O. labronica. In this paper, we examine variations in a number of life-history traits and upper and lower thermal limits across a broad range of acclimation temperatures (10–35 °C) in a laboratory strain of O. labronica, and assess the occurrence and direction of co-variation and trade-off between life-history traits and thermal limits, ultimately exploring their functional or evolutionary significance.
Section snippets
Animal collection, culturing, and experiment preparation
Three hundred individuals of a laboratory strain of O. labronica were used to start the culture employed in our study, which was undertaken at the Marine Biology and Ecology Research Centre of the Plymouth University (Plymouth, UK). This strain derived from 40 individuals (25 females and 15 males) originally collected in the harbour of Grado (Northern Adriatic, Italy; 45°40′N, 13°23′E) in 2007, and kept for approximately 20 generations at room temperature (20 ± 3 °C) and constant salinity (32 ± 2).
Effect of temperature on survival and life history
Preliminary analyses showed that size at the beginning of the exposure time was similar among treatments for males (12.90 ± 0.17 chaetigers; F6,311 = 2.07; P = 0.06); whilst for females significant differences among treatment were found (15.23 ± 0.36 chaetigers; F6,311 = 11.31; P < 0.0001). This result was, however, simply due to the fact that females in the 35 °C treatment were 1 chaetiger smaller, a negligible difference considering that this treatment was not used in the analyses, as it was shortly
Discussion
In order to understand the evolutionary processes underlying adaptation to different temperature regimes we need to investigate the plastic response of a wide spectrum of traits and the direction of their relationships, with particular attention to trade-offs that may constrain evolutionary changes (Stearns, 1992). Our results demonstrate that in the marine polychaete O. labronica a number of life-history and thermal tolerance traits show different temperature-dependent patterns of acclimation:
Acknowledgements
We thank Ann Torr, Roger Haslam and Richard Ticehurst for technical assistance and Andy Foggo for his help in statistical analyses. This work was carried out while Dr. Piero Calosi was in receipt of an RCUK Research Fellowship. Dr. Gloria Massamba N'Siala acknowledges the University of Modena and Reggio Emilia, which has supported this study by providing her a Travelling Fellowship (Mobility Grant 2008). Finally, we would like to thank the three anonymous reviewers, whose constructive critiques
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2023, Oceanography and Marine Biology: An Annual Review, Volume 61