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Extreme Intraclutch Egg-Size Dimorphism in Eudyptes Penguins, an Evolutionary Response to Clutch-Size Maladaptation

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Extreme Intraclutch Egg-Size Dimorphism in Eudyptes Penguins, an Evolutionary Response to Clutch-Size Maladaptation The University of Chicago Extreme Intraclutch Egg-Size Dimorphism in Eudyptes Penguins, an Evolutionary Response to Clutch-Size Maladaptation. Author(s): R. Will Stein and Tony D. Williams Source: The American Naturalist, Vol. 182, No. 2 (August 2013), pp. 260-270 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/10.1086/670929 . Accessed: 13/01/2015 17:34 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press, The American Society of Naturalists, The University of Chicago are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist. http://www.jstor.org This content downloaded from 142.58.26.133 on Tue, 13 Jan 2015 17:34:22 PM All use subject to JSTOR Terms and Conditions vol. 182, no. 2 the american naturalist august 2013 Extreme Intraclutch Egg-Size Dimorphism in Eudyptes Penguins, an Evolutionary Response to Clutch-Size Maladaptation R. Will Stein* and Tony D. Williams Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia V5A 1S6, Canada Submitted December 7, 2011; Accepted March 8, 2013; Electronically published June 5, 2013 Dryad data: http://dx.doi.org/10.5061/dryad.cd233. Roff 2002). Classical life-history theory assumes that traits abstract: Eudyptes penguins (six species) are uniquely character- with clear, direct links to fitness, such as clutch size, are ized by a two-egg clutch with extreme intraclutch egg-size dimor- phism (ESD): the first-laid A-egg is 17.5%–56.9% smaller than the optimized by natural selection (Charlesworth 1994; Roff B-egg. Although A-eggs are viable, they almost never produce fledged 2002). However, a lack of standing phenotypic variation chicks (genus average !1%). Using classical life-history theory and (e.g., most pelagic seabird species have small, invariant phylogenetic comparative methods, we demonstrate a marked slow- clutch sizes of one or two eggs; Hamer et al. 2002) could down in the life history of Eudyptes: age of first reproduction is 52% impede trait optimization (Crespi 2000). Evolutionary sta- later and annual fecundity 48% lower compared with other two-egg sis, including clutch-size invariance in pelagic seabirds, has clutch penguin species. All six Eudyptes species have retained a two- egg clutch, despite this pronounced life-history slowdown; this sug- been explained by persistent stabilizing selection leading gests evolutionary mismatch between clutch size and chicks fledged to constraints mediated by selection (Stearns 1986). Se- per clutch. Consistent with this, we show that Eudyptes fledge 43% lective constraints are considered weak forms of evolu- fewer chicks per clutch than other two-egg clutch penguin species. tionary constraint because constraint is enforced by se- Extreme intraclutch ESD in Eudyptes is associated primarily with a lection, not by the nonrandom production of variants uniform (5%) increase in relative B-egg size, and B-egg size has (Schwenk 1995). Constraints maintained by relatively evolved in accord with life history. We further show that intraclutch ESD is positively correlated with age of first reproduction in Eudyptes weak stabilizing selection relax when selection pressures but not in other two-egg clutch penguin species. We argue that shift; however, strong and persistent selection can lead to Eudyptes’ persistent failure to evolve a one-egg clutch constitutes a trait canalization (Charlesworth et al. 1982; Stearns 1986). unique genus-wide evolutionary maladaptation and that extreme in- If the clutch-size invariance typical of pelagic seabirds re- traclutch ESD evolved as a correlated response to selection favoring sulted from canalization, then this could constrain clutch- a slower life history imposed by their extreme pelagic overwintering size evolution and lead to maladaptation (Crespi 2000). and migration ecology. Pelagic seabirds have slow life histories (small invariant clutch sizes, low annual fecundity, and deferred repro- Keywords: Eudyptes, intraclutch egg-size dimorphism, life-history duction) that are shaped, in part, by the large incremental evolution, maladaptation, selective constraint, Spheniscidae. costs associated with provisioning chicks (Weimerskirch 2002). This cost of reproduction can limit annual fecundity Introduction by negatively impacting adult survival and by exerting strong, persistent stabilizing selection on clutch size (Wei- Life histories encompass the major demographic traits as- merskirch 2002). Penguins (Spheniscidae) have the slow sociated with fitness and describe variation in schedules life histories typical of pelagic seabirds, even though most for growth, survival, and reproduction (Stearns 1992). penguin species are inshore forgers (Williams 1995). Part Life-history trajectories evolve in response to age-specific of the reason for this is that penguins are flightless, and mortality schedules but are constrained by trade-offs and flipper-propelled swimming is an expensive means of evolutionary history (Stearns 1992; Charlesworth 1994; transport. Despite these higher relative transportation * Corresponding author; e-mail: [email protected]. costs, Eudyptes penguins (six species) evolved novel pelagic overwintering behavior that involves a temporally and en- Am. Nat. 2013. Vol. 182, pp. 260–270. ᭧ 2013 by The University of Chicago. 0003-0147/2013/18202-53502$15.00. All rights reserved. ergetically demanding prebreeding migration (Bost et al. DOI: 10.1086/670929 2009; Green et al. 2009). Eudyptes penguins are further This content downloaded from 142.58.26.133 on Tue, 13 Jan 2015 17:34:22 PM All use subject to JSTOR Terms and Conditions Extreme Intraclutch Egg-Size Dimorphism 261 characterized by a form of intraclutch egg-size dimor- intraclutch ESD is correlated with deferred onset of re- phism (ESD) that is unique (first-laid A-egg is smaller) production (mean age of first reproduction) in Eudyptes and extreme (range, 17.5%–56.9%) among birds (Slags- but not in other two-egg clutch penguin species. vold et al. 1984; Williams 1995). In Eudyptes, extreme Our analysis provides support for the interpretation that intraclutch ESD is coupled with systematic loss of the A- Eudyptes’ two-egg clutch is maladaptive (sensu Crespi egg, which is viable (Williams 1990; Davis and Renner 2000). This raises a second question: what might be pre- 2003; Poisbleau et al. 2008) but almost always fails to cluding clutch-size optimization? Constraint-based expla- produce a fledged chick (genus average !1%; Williams nations are subject to criticism because it is always possible 1995). Early, systematic loss of A-eggs or A-chicks is as- to postulate a rare selective regime where a putatively mal- sured by obligate clutch and brood reduction tactics that adaptive trait could be adaptive (Schwenk 1995). For ex- favor B-eggs (St. Clair 1992, 1996; St. Clair et al. 1995). ample, it is plausible that an invariant two-egg clutch cou- In Eudyptes schlegeli (royal penguin), A-eggs are lost at or pled with extreme intraclutch ESD could be advantageous before the time B-eggs are laid; this systematic, early loss during infrequent periods of superabundant resources as- of A-eggs has been attributed to maternal egg ejection and sociated with a long-term (decadal or greater) environ- interpreted as maternal infanticide (St. Clair et al. 1995). mental cycle. Acknowledging this possibility, we suggest Eudyptes penguins appear to sacrifice the time and energy that constraint on clutch-size reduction might be related invested in A-egg production, and this suggests that their to an interaction between the physiology of follicle (yolk) two-egg clutch is maladaptive. development and Eudyptes’ unique pelagic nonbreeding Extreme intraclutch ESD in Eudyptes has defied expla- and migration ecology (see “Discussion”). nation, despite more than 50 years of research (Lack 1968; Johnson et al. 1987; Williams 1990; St. Clair 1992, 1998; Material and Methods St. Clair et al. 1995). The many hypotheses advanced in explanation have focused on adaptive functions for the The Spheniscidae includes the six genera and 18 species smaller A-egg; however, the primary candidate hypothe- of extant penguins (Baker et al. 2006; fig. 1), which exhibit ses—brood reduction (Lack 1954) and insurance against substantial variation in body mass and life-history char- B-egg loss (Dorward 1962)—have not received empirical acteristics (1–24 kg; Williams 1995). The two largest spe- support (Slagsvold et al. 1984; St. Clair et al. 1995). These cies (Aptenodytes; 10–24 kg) first reproduce at 5–6 years, hypotheses emphasize intraclutch ESD, not clutch size. do so once a year or once every other year, and have a Alternatively, we propose that extreme intraclutch ESD one-egg clutch (Williams 1995). The two smallest species evolved as a correlated response to selection favoring a (Eudyptula; 1 kg) first reproduce at 2–3 years, do so once slower life history imposed by Eudyptes’ unique pelagic or twice a year, and have a two-egg clutch with nearly overwintering and migration ecology. If life history has equal-sized eggs (Williams 1995). The 14 species of in- slowed down in Eudyptes, then we would expect clutch termediate-sized penguins (Pygoscelis, Spheniscus, Mega- size to decrease from two eggs to one egg, as seen in dyptes, and Eudyptes; 2–6 kg) first breed at 2–8 years, typ- Aptenodytes penguins (Williams 1995). However, all six ically breed once a year, and have a two-egg clutch with species in Eudyptes have retained a two-egg clutch. Here, either nearly equal-sized eggs (all non-Eudyptes)orex- we use classical life-history theory and phylogenetic com- tremely size-dimorphic eggs (Eudyptes).
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