Hurricane-induced selection on the morphology of an island lizard.

Hurricanes are catastrophically destructive. Beyond their toll on human life and livelihoods, hurricanes have tremendous and often long-lasting effects on ecological systems1,2. Despite many examples of mass mortality events following hurricanes3-5, hurricane-induced natural selection has not previously been demonstrated. Immediately after we finished a survey of Anolis scriptus-a common, small-bodied lizard found throughout the Turks and Caicos archipelago-our study populations were battered by Hurricanes Irma and Maria. Shortly thereafter, we revisited the populations to determine whether morphological traits related to clinging capacity had shifted in the intervening six weeks and found that populations of surviving lizards differed in body size, relative limb length and toepad size from those present before the storm. Our serendipitous study, which to our knowledge is the first to use an immediately before and after comparison6 to investigate selection caused by hurricanes, demonstrates that hurricanes can induce phenotypic change in a population and strongly implicates natural selection as the cause. In the decades ahead, as extreme climate events are predicted to become more intense and prevalent7,8, our understanding of evolutionary dynamics needs to incorporate the effects of these potentially severe selective episodes9-11.

Nature, Data, and Power: How Hegemonies Shaped This Special Section.

AbstractSystems of oppression-racism, colonialism, misogyny, cissexism, ableism, heteronormativity, and more-have long shaped the content and practice of science. But opportunities to reckon with these influences are rarely found within academic science, even though such critiques are well developed in the social sciences and humanities. In this special section, we attempt to bring cross-disciplinary conversations among ecology, evolution, behavior, and genetics on the one hand and critical perspectives from the social sciences and humanities on the other into the pages-and in front of the readers-of a scientific journal. In this introduction to the special section, we recount and reflect on the process of running this cross-disciplinary experiment to confront harms done in the name of science and envision alternatives.

Model Systems in Ecology, Evolution, and Behavior: A Call for Diversity in Our Model Systems and Discipline.

AbstractEcologists and evolutionary biologists are fascinated by life's variation but also seek to understand phenomena and mechanisms that apply broadly across taxa. Model systems can help us extract generalities from amid all the wondrous diversity, but only if we choose and develop them carefully, use them wisely, and have a range of model systems from which to choose. In this introduction to the Special Feature on Model Systems in Ecology, Evolution, and Behavior (EEB), we begin by grappling with the question, What is a model system? We then explore where our model systems come from, in terms of the skills and other attributes required to develop them and the historical biases that influence traditional model systems in EEB. We emphasize the importance of communities of scientists in the success of model systems-narrow scientific communities can restrict the model organisms themselves. We also consider how our discipline was built around one type of "model scientist"-a history still reflected in the field. This lack of diversity in EEB is unjust and also narrows the field's perspective, including by restricting the questions asked and talents used to answer them. Increasing diversity, equity, and inclusion will require acting at many levels, including structural changes. Diversity in EEB, in both model systems and the scientists who use them, strengthens our discipline.

Female-Biased Sex Ratios Increase Colony Survival and Reproductive Output in the Spider Anelosimus studiosus.

Negative frequency-dependent selection acting on the sexes is hypothesized to drive populations toward a balanced sex ratio. However, numerous examples of female-biased sex ratios pepper the arthropods. Theoretical examinations have proposed that female-biased populations or groups can have higher chances of surviving and propagating that may be advantageous. We evaluated this hypothesis in the semisocial spider Anelosimus studiosus by creating artificial colonies of varying sex ratios and sizes and observing colony performance at sites with high versus low group extinction rates. We also tested whether colony extinction rates and sex ratios were correlated across 25 collection sites, spanning 10° latitude. We found that colonies with female-biased sex ratios produced more egg cases and were more likely to survive the duration of a field season, suggesting that female-biased sex ratios confer both survival and reproductive advantages on colonies. The effect of sex ratio on colony survival and reproductive output was strongest for small colonies in high extinction areas. Moreover, we found that female-biased sex ratios correlated with greater extinction rates across 25 sites, indicating that female-biased sex ratios may have evolved at some sites in response to high extinction rates. These findings suggest that selection favoring groups with female-biased sex ratios may operate in A. studiosus, shedding light on some of the factors that may drive the evolution of biased sex ratios.

Estimating encounter rates as the first step of sexual selection in the lizard Anolis sagrei.

How individuals move through their environment dictates which other individuals they encounter, determining their social and reproductive interactions and the extent to which they experience sexual selection. Specifically, females rarely have the option of mating with all males in a population-they can only choose among the males they encounter. Further, quantifying phenotypic differences between the males that females encounter and those that sire females' offspring lends insight into how social and reproductive interactions shape male phenotypes. We used an explicitly spatio-temporal Markov chain model to estimate the number of potential mates of Anolis sagrei lizards from their movement behaviour, and used genetic paternity assignments to quantify sexual selection on males. Females frequently encountered and mated with multiple males, offering ample opportunity for female mate choice. Sexual selection favoured males that were bigger and moved over larger areas, though the effect of body size cannot be disentangled from last-male precedence. Our approach corroborates some patterns of sexual selection previously hypothesized in anoles based on describing them as territorial, whereas other results, including female multiple mating itself, are at odds with territorial polygyny, offering insight into discrepancies in other taxa between behavioural and genetic descriptions of mating systems.

Floral size and shape evolution following the transition to gender dimorphism.

PREMISE OF THE STUDY: Floral morphology is expected to evolve following the transition from cosexuality to gender dimorphism in plants, as selection through male and female function becomes dissociated. Specifically, male-biased dimorphism in flower size can arise through selection for larger flowers through male function, selection for smaller flowers through female function, or both. The evolutionary pathway to floral dimorphism can be most effectively reconstructed in species with intraspecific variation in sexual system. We examined the evolution of flower size and shape in Lycium californicum, whose populations are either gender dimorphic with male and female plants, or cosexual with hermaphroditic plants. METHODS: Floral morphology was characterized in populations spanning the species' complete range. For a subset of the range where cosexual and dimorphic populations are in close proximity, we compared the size and shape of flowers from female and male plants in dimorphic populations to hermaphrodites in cosexual populations, accounting for variation associated with abiotic environmental conditions. KEY RESULTS: The magnitude of flower size dimorphism varied across dimorphic populations. After controlling for environmental variation across cosexual and dimorphic populations, flowers on males were larger than flowers on females and hermaphrodites, whereas flower size did not differ between females and hermaphrodites. Flower shape differences were associated with mating type, sexual system, and environmental variation. CONCLUSIONS: While abiotic environmental gradients shape both overall flower size and shape, male-biased flower size dimorphism in L. californicum appears to arise through selection for larger flowers in males but not smaller flowers in females.

Correlated polymorphism in cytotype and sexual system within a monophyletic species, Lycium californicum.

BACKGROUND AND AIMS: Polyploidy has important effects on reproductive systems in plants and has been implicated in the evolution of dimorphic sexual systems. In particular, higher ploidy is associated with gender dimorphism across Lycium species (Solanaceae) and across populations within the species Lycium californicum. Previous research on the association of cytotype and sexual system within L. californicum sampled a limited portion of the species range, and did not investigate evolutionary transitions between sexual systems. Lycium californicum occurs in arid regions on offshore islands and mainland regions in the south-western United States and Mexico, motivating a more comprehensive analysis of intraspecific variation in sexual system and cytotype across the full range of this species. METHODS: Sexual system (dimorphic vs. cosexual) was determined for 34 populations across the geographical range of L. californicum using field observations of pollen production, and was confirmed using morphological measurements and among-plant correlations of primary sexual traits. Ploidy was inferred using flow cytometry in 28 populations. DNA sequence data from four plastid and two nuclear regions were used to reconstruct relationships among populations and to map transitions in sexual system and ploidy. KEY RESULTS: Lycium californicum is monophyletic, ancestrally diploid and cosexual, and the association of gender dimorphism and polyploidy appears to have two evolutionary origins in this species. Compared with cosexual populations, dimorphic populations had bimodal anther size distributions, negative correlations between male and female floral traits, and larger coefficients of variation for primary sexual traits. Flow cytometry confirmed tetraploidy in dimorphic populations, whereas cosexual populations were diploid. CONCLUSIONS: Tetraploidy and gender dimorphism are perfectly correlated in L. californicum, and the distribution of tetraploid-dimorphic populations is restricted to populations in Arizona and the Baja California peninsula. The analysis suggests that tetraploidy and dimorphism likely established in Baja California and may have evolved multiple times.

Out of America to Africa or Asia: inference of dispersal histories using nuclear and plastid DNA and the S-RNase self-incompatibility locus.

The plant genus Lycium (Solanaceae) originated in the Americas and includes approximately 85 species that are distributed worldwide. The vast majority of Old World species occur in southern Africa and eastern Asia. In this study, we examine biogeographic relationships among Old World species using a phylogenetic approach coupled with molecular evolutionary analyses of the S-RNase self-incompatibility gene. The phylogeny inferred from nuclear granule-bound starch synthase I (GBSSI), nuclear conserved ortholog set II (COSII) marker C2_At1g24360, and plastid spacer data (trnH-pbsA, trnD(GUC)-trnT(GGU), rpl32-trnL(UAG), and ndhF-rpl32) includes a clade of eastern Asian Lycium nested within the African species, suggesting initial dispersal from the Americas to Africa, with subsequent dispersal to eastern Asia. Molecular dating estimates suggest that these dispersal events occurred relatively recently, with dispersal from the Americas to Africa approximately 3.64 Ma (95% highest posterior density [HPD]: 1.58-6.27), followed by subsequent dispersal to eastern Asia approximately 1.21 Ma (95% HPD: 0.32-2.42). In accordance, the S-RNase genealogy shows that S-RNases isolated from Old World species are restricted to four lineages, a subset of the 14 lineages including S-RNases isolated from New World Lycium species, supporting a bottleneck of S-RNase alleles concomitant with a single dispersal event from the Americas to the Old World. Furthermore, the S-RNase genealogy is also consistent with dispersal of Lycium from Africa to Asia, as eastern Asian alleles are restricted to a subset of the lineages that also include African alleles. Such a multilocus approach, including complementary data from GBSSI, COSII, plastid spacer regions, and S-RNase, is powerful for understanding dispersal histories of closely related species.

Male and female Anolis carolinensis maintain their dimorphism despite the presence of novel interspecific competition.

Natural selection favors sexual dimorphism that reduces resource competition between the sexes of the same species. However, niche partitioning among interspecific competitors should counter such divergence, as partitioning the niche results in smaller total niche widths for each individual species, leaving less room for the sexes to diverge. A straightforward (and long-standing) hypothesis emerges: species in competitor-rich ecological communities should show less sexual dimorphism than species in competitor-poor ecological communities. Here, we test this prediction using a well-documented natural experiment generated by the recent arrival of Anolis sagrei to a set of small islands in Mosquito Lagoon, Florida, containing Anolis carolinensis. Despite known interspecific habitat partitioning and rapid evolution in habitat-use traits by A. carolinensis in this system, sexual dimorphism between male and female A. carolinensis was not reduced as predicted on two-species islands relative to islands with only A. carolinensis. This is consistent with a small but growing body of empirical tests of the dimorphism-richness hypothesis that have been ambiguous in their support at best. A rethinking of the validity of this intuitive hypothesis is needed.

What Determines Paternity in Wild Lizards? A Spatiotemporal Analysis of Behavior and Morphology.

Mating behavior in animals can be understood as a sequence of events that begins with individuals encountering one another and ends with the production of offspring. Behavioral descriptions of animal interactions characterize early elements of this sequence, and genetic descriptions use offspring parentage to characterize the final outcome, with behavioral and physiological assessments of mates and mechanisms of copulation and fertilization comprising intermediate steps. However, behavioral and genetic descriptions of mating systems are often inconsistent with one another, complicating expectations for crucial aspects of mating biology, such as the presence of multiple mating. Here, we use behavioral and genetic data from a wild population of the lizard Anolis cristatellus to characterize female multiple mating and the potential for sexual selection through female mate choice in this species. We find that 48% of sampled females bore offspring sired by multiple males. Moreover, spatiotemporal proximity between males and females was associated with whether a male sired a female's offspring, and if yes, how many offspring he sired. Additionally, male body size, but not display behavior, was associated with reproductive outcomes for male-female pairs. While much remains to be learned about the mechanisms of mating and targets of sexual selection in A. cristatellus, it is clear that female multiple mating is a substantial component of this species' mating system in nature.

Author Correction: An alternative hypothesis for the evolution of same-sex sexual behaviour in animals.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Character displacement in the midst of background evolution in island populations of Anolis lizards: A spatiotemporal perspective.

Negative interactions between species can generate divergent selection that causes character displacement. However, other processes cause similar divergence. We use spatial and temporal replication across island populations of Anolis lizards to assess the importance of negative interactions in driving trait shifts. Previous work showed that the establishment of Anolis sagrei on islands drove resident Anolis carolinensis to perch higher and evolve larger toepads. To further test the interaction's causality and predictability, we resurveyed a subset of islands nine years later. Anolis sagrei had established on one island between surveys. We found that A. carolinensis on this island now perch higher and have larger toepads. However, toepad morphology change on this island was not distinct from shifts on six other islands whose Anolis community composition had not changed. Thus, the presence of A. sagrei only partly explains A. carolinensis trait variation across space and time. We also found that A. carolinensis on islands with previously established A. sagrei now perch higher than a decade ago, and that current A. carolinensis perch height is correlated with A. sagrei density. Our results suggest that character displacement likely interacts with other evolutionary processes in this system, and that temporal data are key to detecting such interactions.

An alternative hypothesis for the evolution of same-sex sexual behaviour in animals.

Same-sex sexual behaviour (SSB) has been recorded in over 1,500 animal species with a widespread distribution across most major clades. Evolutionary biologists have long sought to uncover the adaptive origins of 'homosexual behaviour' in an attempt to resolve this apparent Darwinian paradox: how has SSB repeatedly evolved and persisted despite its presumed fitness costs? This question implicitly assumes that 'heterosexual' or exclusive different-sex sexual behaviour (DSB) is the baseline condition for animals, from which SSB has evolved. We question the idea that SSB necessarily presents an evolutionary conundrum, and suggest that the literature includes unchecked assumptions regarding the costs, benefits and origins of SSB. Instead, we offer an alternative null hypothesis for the evolutionary origin of SSB that, through a subtle shift in perspective, moves away from the expectation that the origin and maintenance of SSB is a problem in need of a solution. We argue that the frequently implicit assumption of DSB as ancestral has not been rigorously examined, and instead hypothesize an ancestral condition of indiscriminate sexual behaviours directed towards all sexes. By shifting the lens through which we study animal sexual behaviour, we can more fruitfully examine the evolutionary history of diverse sexual strategies.

Collective behavior and colony persistence of social spiders depends on their physical environment.

The physical environment occupied by group-living animals can profoundly affect their cooperative social interactions and therefore their collective behavior and success. These effects can be especially apparent in human-modified habitats, which often harbor substantial variation in the physical environments available within them. For nest-building animal societies, this influence of the physical environment on collective behavior can be mediated by the construction of nests-nests could either buffer animal behavior from changes in the physical environment or facilitate shifts in behavior through changes in nest structure. We test these alternative hypotheses by examining the differences in collective prey-attacking behavior and colony persistence between fence-dwelling and tree-dwelling colonies of Stegodyphus dumicola social spiders. Fences and trees represent substantially different physical environments: fences are 2-dimensional and relatively homogenous environments, whereas tree branches are 3-dimensional and relatively heterogeneous. We found that fence-dwelling colonies attack prey more quickly and with more attackers than tree-dwelling colonies in both field and controlled settings. Moreover, in the field, fence-dwelling colonies captured more prey, were more likely to persist, and had a greater number of individuals remaining at the end of the experiment than tree-dwelling colonies. Intriguingly, we also observed a greater propensity for colony fragmentation in tree-dwelling colonies than fence-dwelling colonies. Our results demonstrate that the physical environment is an important influence on the collective behavior and persistence of colonies of social spiders, and suggest multiple possible proximate and ultimate mechanisms-including variation in web complexity, dispersal behavior, and bet-hedging-by which this influence may be realized.

Selection for Collective Aggressiveness Favors Social Susceptibility in Social Spiders.

Particularly socially influential individuals are present in many groups [1-8], but it is unclear whether their emergence is determined by their social influence versus the social susceptibility of others [9]. The social spider Stegodyphus dumicola shows regional variation in apparent leader-follower dynamics. We use this variation to evaluate the relative contributions of leader social influence versus follower social susceptibility in driving this social order. Using chimeric colonies that combine potential leaders and followers, we discover that leader-follower dynamics emerge from the site-specific social susceptibility of followers. We further show that the presence of leaders increases colony survival in environments where leader-follower dynamics occur. Thus, leadership is driven by the "social susceptibility" of the population majority, rather than the social influence of key group members.

Does ecological specialization transcend scale? Habitat partitioning among individuals and species of Anolis lizards.

Ecological specialization is common across all levels of biological organization, raising the question of whether the evolution of specialization at one scale in a taxon is linked to specialization at other scales. Anolis lizards have diversified repeatedly along axes of habitat use, but it remains unknown if this diversification into habitat use specialists is underlain by individual specialization. From repeated observations of individuals in a population of Anolis sagrei in Florida, we show that the extent of habitat use specialization among individuals is comparable to the extent of specialization in the same traits among ten sympatric Anolis habitat specialist species in Cuba. However, the adaptive correlations between habitat use and morphology commonly seen across species of Anolis were not observed across individuals in the sampled population. Our results therefore suggest that while patterns of ecological specialization can transcend scale, these parallels are the consequence of distinct ecological processes acting at microevolutionary and macroevolutionary scales.

Intraindividual Behavioral Variability Predicts Foraging Outcome in a Beach-dwelling Jumping Spider.

Animal personality, defined as consistent differences between individuals in behavior, has been the subject of hundreds if not thousands of papers. However, little work explores the fitness consequences of variation in behavior within individuals, or intraindividual variability (IIV). We probe the effects of behavioral IIV on predator-prey interaction outcomes in beach-dwelling jumping spiders (Terralonus californicus). Prior studies have found that spiders with higher body condition (body mass relative to size) behave more variably. Thus, we hypothesized that jumping spider activity level IIV would relate positively to foraging performance. To address this, we tested for associations between activity IIV, average activity level, and two measures of foraging success in laboratory mesocosms: change in spider mass and the number of prey killed. Activity IIV positively correlated with the mass that spiders gained from prey, but not with the number of prey killed. This suggests that spiders with high IIV consumed a greater proportion of their prey or used less energy. Interestingly, average activity level (personality) predicted neither metric of foraging success, indicating that behavioral IIV can predict metrics of success that personality does not. Therefore, our findings suggest that IIV should be considered alongside personality in studies of predator-prey interactions.