In Memoriam: Barry Sinervo 1961–2021

In March 2021, evolutionary biologist and ecologist Professor Barry Sinervo at University of California Santa Cruz (UCSC) passed away at the age of 60, after a brave struggle with cancer (Fig. 1). Barry is mourned by his wife of 32 years Jeanie Vogelzang, his son Ari Sinervo, and other family members. His premature death has also caused much sorrow among his departmental colleagues at UCSC, scientific collaborators around the world, and former students and postdocs, including the authors of the current piece. Here, we summarize Barry's scientific achievements, discuss his legacy, and provide some personal memories of our interactions with him when carrying out research in his laboratory. Those of us writing this article are former postdocs and PhD students who all spent considerable time in Barry's laboratory, and we wish to share some of the intellectual excitement we experienced during these formative years of our academic careers. Together, our team covers a large time span of Barry's faculty career, and the authors of this piece include Barry's first PhD student (R.C.), his first European postdoc (E.I.S), his last PhD student (P.B.) as well as his co-workers, students, and laboratory members in between these periods (A.M.A., L.L., and S.C.M.), from 1997 and onwards. Barry started his scientific career by earning a B.Sc. in biology and mathematics at Dalhousie University in Nova Scotia. He then joined the Department of Zoology at Washington University, under the supervision of Professor Raymond Huey. It was during these early formative years that Barry developed the classical experimental protocols that would subsequently establish him as a young and rising star in evolutionary biology: experimental techniques to manipulate egg and offspring size, that he termed “allometric engineering.” By experimentally removing part of the yolk from eggs of two species of sea urchins (Strongolycentrotus) and later also Western Fence Lizards (Scleroporos occidentalis) and side-blotched lizards (Uta stansburiana), Barry and his colleagues explored the fitness and performance consequences of maternal effects and early developmental history on offspring (Fig. 1B). This pioneering experimental work resulted in a series of classic and highly influential papers published in Evolution and Science (Sinervo and McEdward 1988; Sinervo 1990; Sinervo and Huey 1990; Sinervo et al. 1992). Barry's early work illustrates his interest in both development and ecology, and how a knowledge of both fields is crucial to understand evolution. Barry was an early pioneer in linking ecology to development and evolution, well before the later rapid growth of evolutionary developmental biology (“evo-devo”) as an emerging and increasingly popular research topic. Barry's experimental manipulations of offspring size revealed the mechanistic links between size and offspring performance, including how ecologically important traits like sprint speed are important for lizards to escape predators and the general importance of allometric size-performance relationships. These classical experimental phenotypic manipulations also revealed the importance of early environmental effects and offspring development, which many biologists nowadays appreciate as being fundamental to understand both ecological and evolutionary dynamics of natural populations. It provided the foundation that established him as a truly integrative evolutionary biologist. This work also earned him the Society for the Study of Evolution's (SSE) Theodosius Dobzhansky Prize in 1992, and a Young Investigator Award from the American Society of Naturalists. Interestingly, Barry's advisor Ray Huey did not believe that these experimental manipulations would work and advised him against doing them, but he was happy to be proven wrong when they turned out successful (R. Huey, pers. commun.). This episode underscores that PhD students should not always follow the advice of senior supervisors and that pushing through ideas you really believe in can lead to scientific innovations. After defending his PhD in Seattle, Barry subsequently moved to UC Berkeley, where he obtained the prestigious Miller postdoctoral fellowship, working with the endocrinologist Professor Paul Licht. During this time in Berkeley, Barry developed his interests in the mechanistic and developmental basis of life-history variation. He designed experimental endocrinological manipulations on female side-blotched lizards with the aim of understanding the trade-off between egg quantity and egg quality. By experimentally manipulating circulating levels of follicle-stimulating hormone (FSH) in females, he showed in a paper in Journal of Experimental Zoology that this hormone had pleiotropic effects on both traits: it simultaneously increased egg number and decreased egg size as a correlated effect (Sinervo and Licht 1991a). This was a groundbreaking experiment that resulted in a paper in Science (Sinervo and Licht 1991b) and which established a concrete and mechanistic proof-of-principle of the theory that life-history trade-offs were likely to emerge as a result of antagonistic pleiotropy of genes with effects on several different traits, as discussed in a later publication by Barry in American Naturalist (Sinervo 1999). After obtaining faculty positions as professor, first in Bloomington at Indiana University and subsequently at UCSC, Barry continued to study side-blotched lizards in an individually marked field population at Los Baños (Merced County) in California (Fig. 1C). He chose this study location after driving around a large part of California, scouting out different sites that would be suitable for a long-term population study of marked individuals. Once Barry had settled on the field site at Los Baños, he continued to use his experimental techniques and applied them in the field, aiming to understand how natural selection shaped life-history evolution in a realistic ecological setting. The landscape at Los Baños is characterized by dry, grassy areas and rolling hills, where enormous numbers of lizards live in high density on semi-isolated rocky outcroppings (Fig. 1C). Although these little animals are fleet of foot (Barry would have called them “wiley”), he had mastered the art of capture and routinely captured and processed more than 100 individuals per day. Those of us who participated in the field work at Los Baños often participated in daily competition with Barry to catch as many lizards as he did, but he was typically able to catch more than the rest of the team combined during a whole day, which says a lot about his outstanding skills as a field biologist. It was after several years of field work at Los Baños that Barry discovered and described the evolutionary and social dynamics leading to perhaps his most famous paper in Nature in 1996: “The rock-paper-scissors game and the evolution of alternative male strategies” (Sinervo and Lively 1996) (Fig. 1D). Together with his colleague Curtis Lively (still at Indiana University), they described three heritable male throat color morphs that persist in this population, while fluctuating in their relative frequencies every generation (Sinervo and Lively 1996). Based on field data and game theoretical modeling, Barry and Curt argued that this polymorphism was maintained by a particular form of negative frequency-dependent selection (NFDS), namely a rock-paper-scissor game (RPS), in which the different morphs showed intransitive fitnesses, each morph having its own strengths and weaknesses in intrasexual selection and competition over access to females and mating opportunities (Maynard Smith 1996). RPS had previously been a theoretical idea, explored by the evolutionary theorist John Maynard Smith, but here was a possible case of its operation and existence in a natural population in the wild. It is fair to say that the RPS-paper was met with some skepticism by many evolutionary biologists and the idea does not seem to have had a big impact on the field of behavioral ecology. However, outside of behavioral ecology, intransitive fitnesses in general, and the RPS-paper in particular, have had a huge impact in fields like theoretical evolutionary biology, biodiversity, adaptive radiations, community ecology, evolutionary genetics, and microbial experimental evolution (Rainey and Travisano 1998; Palumbi 1999; Czárán et al. 2002; Kerr et al. 2002; Zhang et al. 2013; Arnold 2020). We strongly suspect one reason why behavioral ecologists have not fully embraced the concept of intransitive fitnesses and the RPS is a cultural barrier: in the behavioral ecology tradition, there is often a strong focus on evolutionary endpoints and optima, rather than on the dynamics of the evolutionary process. To be fair, Barry had a tendency to oversell the RPS, and the dynamical complexity within Barry's conceptual evolutionary models sometimes became intractable. Barry strongly rejected simpler concepts such as indirect genetic effects (IGE) arising from social and parental interactions (Wolf et al. 2001) that could potentially explain the observed patterns. Barry claimed that these more simplified approaches sacrificed mechanistic insight to tractability at the cost of understanding. This position reflects Barry's integrative approach, which aimed to merge genetics, development, physiology, and mathematics to understand the evolutionary process. Barry therefore did not shrink from complexity and attempted to understand rather than minimize its impact. The last words about the RPS and the male color polymorphism have probably not been said, but we strongly suspect that Barry got the major picture right about how this and other forms of enigmatic behavioral polymorphisms are maintained. In 1998, interested in studying dispersal in the side-blotched lizards, Barry visited Jean Clobert in Paris. Barry and Jean immediately had passionate discussions about how dispersal could be linked with the three color morph system. Barry visited Jean's captive common lizards at Foljuif (south of Paris) and to Jean's surprise they discovered that female common lizards also displayed some color morphs. From this first encounter, a long-term collaboration between Barry and Jean was established primarily focused on color morphs, the role of corticosterone, and the effects of climate change. In common with many of us, Jean has data and experiments that he carried out with Barry that are still to be published. Jean treasures Barry's personality and will forever remember the intense scientific discussions they had over the years. A common theme in all our memories of Barry is that he was certainly one of the rare people with whom we have had such rich scientific exchanges. Several of us in the group shared Barry's strong interests in maternal effects, and particularly the idea that maternal physiology could be a powerful way to translate social dynamics into offspring developmental trajectories. This work led to a series of papers on the role of early environmental and maternal effects and the effects on phenotypic integration, including how egg size and maternal hormone investment can trigger changes in phenotype to successfully integrate each mating type with effective antipredator strategies (Lancaster et al. 2007, 2010; Paranjpe et al. 2013). This work was strongly facilitated by Barry's curiosity-driven research efforts, aiming to link social environments with physiology and with the aim to understand the complexity of dynamic evolutionary processes. In addition to his papers, Barry also leaves behind a global network of scientists grateful for their time spent interacting with him and others in the vibrant environment he created in his laboratory. The authors of the current piece all spent some of our formative years in Barry's laboratory. The insights we gained by interacting with Barry and other members of the laboratory were instrumental for us in our subsequent research careers. Below, we include some personal anecdotes to provide a general flavor of the unique and extremely creative research environment that we experienced in Barry's laboratory. One of us (E.I.S.) joined Barry's laboratory as a postdoc at UCSC in 1997, when Barry was a young faculty member (36 years) and had just started his position. E.I.S. was Barry's first postdoc, and came from Sweden where he had mainly been exposed to classical behavioral ecology during his PhD. It was somewhat of a cultural and scientific shock being exposed to a new way of thinking in Barry's laboratory, where population genetics, development, and big questions in evolutionary biology were discussed during laboratory meetings and during commutes to the field site at Los Baños. Initially, E.I.S. found himself in doubt over the basic story about the lizard throat color polymorphism and the causes of its evolutionary maintenance, and he was not alone in the laboratory in these feelings. Working with Barry in the field, compiling data and performing experimental investigations gradually convinced E.I.S. that this polymorphism was indeed a real phenomenon in demand of explanation. Together with Barry and several other colleagues in the laboratory, including A.M.A., we also explored the dynamics of the color polymorphism in females, its fitness consequences and genetic background, and documented striking genetic correlations between color, immune function, and life-history traits (Sinervo et al. 2000; Sinervo and Svensson 2002; Svensson et al. 2009). Another one of us (S.C.M.) met Barry while he was in Finland as the external examiner of a PhD thesis in 2002, was encouraged to apply for funding, and would go on to visit his laboratory every spring for 4 years from 2003 to 2006. One year, together with L.T.L. and Donald Miles, we decided to investigate proximate mechanisms behind the behavioral, physiological, and morphological differences of the different color morphs. In true Barry style, we carried out a natural selection experiment in the field, investigating selection on suites of hormone-mediated traits. Rather than manipulating testosterone (T) and corticosterone, Barry was enthusiastic to look at the upstream gonadotropins luteinizing hormone (LH) and follicle-stimulating hormone (FSH) that regulate T to highlight endocrine cascades. Through manipulations of LH and FSH, whose natural expression is thought to be under genetic control, we also showed that the responses to hormones in the different color morphs were at least partly adaptive. For example, the yellow-throated male morph is more plastic and can upregulate these hormones opportunistically, whereas the other morphs lack such plasticity (Mills et al. 2008). Despite the scale of these projects, the laboratory was a well-oiled machine with lizards in multiple coolers arriving to be processed and then returning to the field. Even when S.C.M was isolated at home with TB (which Barry diagnosed in 5 minutes though it had baffled doctors for months), the coolers kept on coming, the doorbell would ring and the cooler would be left there on the doorstep! When P.B. (Barry's last PhD student) told her then herpetology professor, Dr. Jim Archie at Cal State Long Beach that she had been accepted into Barry's laboratory, he dropped everything to give her a huge hug in his excitement for her to enter into the laboratory of one of the greats. Barry's influential RPS work, textbook material in her undergraduate courses, left P.B. feeling slightly intimidated to join a laboratory with such a big name. Although Barry was a big name with big ideas, he had an equally big heart. Barry lived and breathed for the lizards, so much so that even in the trenches of his fight with cancer and in the worst of the COVID pandemic, to preserve the work and isolate himself he lived in an old trailer on the field site itself so he did not have to make the long drives to and from his home. His dedication was admirable. Barry certainly never thought small, and it was exciting to be involved in his large ideas. We try to continue this legacy today and encourage our students not to shy away from whole-organismal performance experiments. We also repeat more trivial but amusing day to day quotes from Barry, such as the five Ps: Prior Planning Prevents Poor Performance, an important classic as Lizard land was a couple of away from the laboratory. Barry also at to such as the time one of us chose a to on in field The was a out of which us of its but to this it Barry's of to Once field had been and Barry's had he with a but and of how that would forever be in her and The formative years in Barry's laboratory our interests in selection for different genetic and phenotypic adaptive landscape theory and its interests in adaptive landscape theory and were also partly by the landscape of the dry, rolling grassy at Los Baños and Barry would often on the long drives to the of the to These long drives were an important for all of us, as they provided rare opportunities to access to Barry, whose of work and were so intense that he was to We to the field site together each day, in Barry's with Barry on the home had of to while the from a long day under the would in a in the Barry was just as happy to about and natural as he was to of his with a in the but in the background, his was always over the of natural selection on the lizards with a result of the vibrant intellectual in Barry's laboratory, E.I.S. and was one of Barry's first PhD some years later a about adaptive together and L.T.L. later the to Sweden became a postdoc in the laboratory of as faculty member at University of in the Barry was and to his was in In in Barry the and the at the of the Society for by his in One of the was certainly as 5 minutes into his Barry was still in Barry was never of to but he and had a huge network of collaborators all over the His laboratory was an and where many long-term and were with his We are grateful for this indirect that Barry had on our research and that more in the but also environment that his laboratory with many and creative and from different of and many other of the E.I.S. and also remember being by Barry to some in evolutionary biology, such as and in particular The and Barry had a of knowledge in the history of ecology and evolutionary biology, including and This knowledge the way he thought about carried out his and his students and During the last part of Barry's career, from and his premature death in March 2021, his research were mainly of climate and its potentially consequences in of increased of populations. Barry and a large team of collaborators from all over the published a highly paper in Science in where they and described the of and of lizards in the of rapid climate and global (Sinervo et al. Barry also influential study the of in the which was also to climate et al. Although the lizard study was later by other who the that of lizard and of species would go by and Barry and his colleagues to these and maintained their (Sinervo et al. time will Barry and his colleagues were but there are other that be in other than lizards and Barry's and with the from climate were one with his about a and of of lizards, his family members encourage all who to Barry's and work to to the climate and which for a and for a to a of it be about how Barry his research on being at his work in more basic in life-history evolution, game and color We have also this and are that he did not these of research as being of but rather as his general in understanding our natural and on this His later work on how and early environmental effects with lizard throat such integrative climate and life-history evolution et al. 2013). Barry was to his research and provide a general of his different research but he was thinking about how to apply game theory to the from a by to a more He was also thinking about how to apply ideas to understand the at that he to E.I.S. in their last in Santa Cruz in We this by that there is a research interest and to how climate and can and the evolution of color polymorphisms (Lancaster et al. et al. Svensson et al. 2020). We are that Barry would have been and by these E.I.S. the first of this on discussions and with from all the other A.M.A., and all to subsequent and of the The authors of

Récupéré en direct depuis OpenAlex et désinversé. Les résumés ne sont pas conservés dans cette base de données : les index inversés représentent 8,6 Go des 9,3 Go de texte de la base, et le serveur dispose de 13 Go libres.