Evidence for individual vocal recognition in a pair-bonding poison frog, Ranitomeya imitator.

Individually distinctive vocalizations are widespread in nature, although the ability of receivers to discriminate these signals has only been explored through limited taxonomic and social lenses. Here, we asked whether anuran advertisement calls, typically studied for their role in territory defense and mate attraction, facilitate recognition and preferential association with partners in a pair-bonding poison frog (Ranitomeya imitator). Combining no- and two-stimulus choice playback experiments, we evaluated behavioral responses of females to male acoustic stimuli. Virgin females oriented to and approached speakers broadcasting male calls independent of caller identity, implying that females are generally attracted to male acoustic stimuli outside the context of a pair bond. When pair-bonded females were presented with calls of a mate and a stranger, they showed significant preference for calls of their mate. Moreover, behavioral responses varied with breeding status: females with eggs were faster to approach stimuli than females that were pair bonded but did not currently have eggs. Our study suggests a potential role for individual vocal recognition in the formation and maintenance of pair bonds in a poison frog and raises new questions about how acoustic signals are perceived in the context of monogamy and biparental care.

Thermal Plasticity in Behavioral Traits Mediates Mating and Reproductive Dynamics in an Ectotherm.

AbstractEnvironmental temperatures potentially influence reproductive performance and sexual selection by restricting opportunities for activity. However, explicit tests of the behavioral mechanisms linking thermal variation to mating and reproductive performance are rare. We address this gap in a temperate lizard by combining social network analysis with molecular pedigree reconstruction in a large-scale thermal manipulation experiment. Populations exposed to cool thermal regimes presented fewer high-activity days compared with populations exposed to a warmer regime. While plasticity in thermal activity responses in males masked overall differences in activity levels, prolonged restriction nevertheless affected the timing and consistency of male-female interactions. Females were less capable than males of compensating for lost activity time under cold stress, and less active females in this group were significantly less likely to reproduce. While sex-biased activity suppression appeared to limit male mating rates, this did not correspond to a heightened intensity of sexual selection or shifts in the targets of sexual selection. In many populations facing thermal activity restriction, sexual selection on males may play a limited role relative to other thermal performance traits in facilitating adaptation.

Evolution of acoustic signals associated with cooperative parental behavior in a poison frog.

The emergence of complex social interactions is predicted to be an important selective force in the diversification of communication systems. Parental care presents a key social context in which to study the evolution of novel signals, as care often requires communication and behavioral coordination between parents and is an evolutionary stepping-stone toward increasingly complex social systems. Anuran amphibians (frogs and toads) are a classic model of acoustic communication and the vocal repertoires of many species have been characterized in the contexts of advertisement, courtship, and aggression, yet quantitative descriptions of calls elicited in the context of parental care are lacking. The biparental poison frog, Ranitomeya imitator, exhibits a remarkable parenting behavior in which females, cued by the calls of their male partners, feed tadpoles unfertilized eggs. Here, we characterized and compared calls across three social contexts, for the first time including a parental care context. We found that egg-feeding calls share some properties with both advertisement and courtship calls but also had unique properties. Multivariate analysis revealed high classification success for advertisement and courtship calls but misclassified nearly half of egg feeding calls as either advertisement or courtship calls. Egg feeding and courtship calls both contained less identity information than advertisement calls, as expected for signals used in close-range communication where uncertainty about identity is low and additional signal modalities may be used. Taken together, egg-feeding calls likely borrowed and recombined elements of both ancestral call types to solicit a novel, context-dependent parenting response.

A quantitative synthesis of and predictive framework for studying winter warming effects in reptiles.

Increases in temperature related to global warming have important implications for organismal fitness. For ectotherms inhabiting temperate regions, 'winter warming' is likely to be a key source of the thermal variation experienced in future years. Studies focusing on the active season predict largely positive responses to warming in the reptiles; however, overlooking potentially deleterious consequences of warming during the inactive season could lead to biased assessments of climate change vulnerability. Here, we review the overwinter ecology of reptiles, and test specific predictions about the effects of warming winters, by performing a meta-analysis of all studies testing winter warming effects on reptile traits to date. We collated information from observational studies measuring responses to natural variation in temperature in more than one winter season, and experimental studies which manipulated ambient temperature during the winter season. Available evidence supports that most reptiles will advance phenologies with rising winter temperatures, which could positively affect fitness by prolonging the active season although effects of these shifts are poorly understood. Conversely, evidence for shifts in survivorship and body condition in response to warming winters was equivocal, with disruptions to biological rhythms potentially leading to unforeseen fitness ramifications. Our results suggest that the effects of warming winters on reptile species are likely to be important but highlight the need for more data and greater integration of experimental and observational approaches. To improve future understanding, we recap major knowledge gaps in the published literature of winter warming effects in reptiles and outline a framework for future research.

Gene expression underlying parenting and being parented shows limited plasticity in response to different ambient temperatures.

Flexible interactions between parents and offspring are essential for buffering families against variable, unpredictable, and challenging environmental conditions. In the subsocial carrion beetle, Nicrophorus orbicollis, mid-summer temperatures impose steep fitness costs on parents and offspring but do not elicit behavioural plasticity in parents. Here, we ask if plasticity of gene expression underpins this behavioural stability or facilitates independent compensation by larvae. To test this, we characterized gene expression of parents and offspring before and during active parenting under benign (20°C) and stressful (24°C) temperatures to identify genes of parents and offspring associated with thermal response, parenting/being parented, and gene expression plasticity associated with behavioural stability of parental care. The main effects of thermal and social condition each shaped patterns of gene expression in females, males, and larvae. In addition, we implicated 79 genes in females as "buffering" parental behaviour across environments. The majority of these underwent significant changes in expression in actively parenting mothers at the benign temperature, but not at the stressful temperature. Our results suggest that neither genetic programmes for parenting nor their effects on offspring gene expression are fundamentally different under stressful conditions, and that behavioural stability is associated primarily with the maintenance of existing genetic programmes rather than replacement or supplementation. Thus, while selection for compensatory gene expression could expand the range of thermal conditions parents will tolerate, without expanding the toolkit of genes involved selection is unlikely to lead to adaptive changes of function.

The thermal environment as a moderator of social evolution.

Animal sociality plays a crucial organisational role in evolution. As a result, understanding the factors that promote the emergence, maintenance, and diversification of animal societies is of great interest to biologists. Climate is among the foremost ecological factors implicated in evolutionary transitions in social organisation, but we are only beginning to unravel the possible mechanisms and specific climatic variables that underlie these associations. Ambient temperature is a key abiotic factor shaping the spatio-temporal distribution of individuals and has a particularly strong influence on behaviour. Whether such effects play a broader role in social evolution remains to be seen. In this review, we develop a conceptual framework for understanding how thermal effects integrate into pathways that mediate the opportunities, nature, and context of social interactions. We then implement this framework to discuss the capacity for temperature to initiate organisational changes across three broad categories of social evolution: group formation, group maintenance, and group elaboration. For each category, we focus on pivotal traits likely to have underpinned key social transitions and explore the potential for temperature to affect changes in these traits by leveraging empirical examples from the literature on thermal and behavioural ecology. Finally, we discuss research directions that should be prioritised to understand the potentially constructive and/or destructive effects of future warming on the origins, maintenance, and diversification of animal societies.

Constrained flexibility of parental cooperation limits adaptive responses to harsh conditions.

Parental care is predicted to evolve to mitigate harsh environments, thus adaptive plasticity of care may be an important response to our climate crisis. In biparental species, fitness costs may be reduced by resolving conflict and enhancing cooperation among partners. We investigated this prediction with the burying beetle, Nicrophorus orbicollis, by exposing them to contrasting benign and harsh thermal environments. Despite measurable fitness costs under the harsh environment, sexual conflict persisted in the form of sex-specific social plasticity. That is, females provided equivalent care with or without males, whereas males with partners deserted earlier and reduced provisioning effort. The interaction of social condition and thermal environment did not explain variation in individual behavior, failing to support a temperature-mediated shift from conflict to cooperation. Examining selection gradients and splines on cumulative care revealed a likely explanation for these patterns. Contrary to predictions, increased care did not enhance offspring performance under stress. Rather, different components of care were under different selection regimes, with optimization constrained due to lack of coordination between parents. We suggest that the potential for parenting to ameliorate the effects of our climate crisis may depend on the sex-specific evolutionary drivers of parental care, and that this may be best reflected in components of care.

Whitefly Endosymbionts: Biology, Evolution, and Plant Virus Interactions.

Whiteflies (Hemiptera: Aleyrodidae) are sap-feeding global agricultural pests. These piercing-sucking insects have coevolved with intracellular endosymbiotic bacteria that help to supplement their nutrient-poor plant sap diets with essential amino acids and carotenoids. These obligate, primary endosymbionts have been incorporated into specialized organs called bacteriomes where they sometimes coexist with facultative, secondary endosymbionts. All whitefly species harbor the primary endosymbiont Candidatus Portiera aleyrodidarum and have a variable number of secondary endosymbionts. The secondary endosymbiont complement harbored by the cryptic whitefly species Bemisia tabaci is particularly complex with various assemblages of seven different genera identified to date. In this review, we discuss whitefly associated primary and secondary endosymbionts. We focus on those associated with the notorious B. tabaci species complex with emphasis on their biological characteristics and diversity. We also discuss their interactions with phytopathogenic begomoviruses (family Geminiviridae), which are transmitted exclusively by B. tabaci in a persistent-circulative manner. Unraveling the complex interactions of these endosymbionts with their insect hosts and plant viruses could lead to advancements in whitefly and whitefly transmitted virus management.

Debugging: Strategies and Considerations for Efficient RNAi-Mediated Control of the Whitefly Bemisia tabaci.

The whitefly Bemisia tabaci is a globally important pest that is difficult to control through insecticides, transgenic crops, and natural enemies. Post-transcriptional gene silencing through RNA interference (RNAi) has shown potential as a pest management strategy against B. tabaci. While genomic data and other resources are available to create highly effective customizable pest management strategies with RNAi, current applications do not capitalize on species-specific biology. This lack of specificity has the potential to have substantial ecological impacts. Here, we discuss both short- and long-term considerations for sustainable RNAi pest management strategies for B. tabaci, focusing on the need for species specificity incorporating both life history and population genetic considerations. We provide a conceptual framework for selecting sublethal target genes based on their involvement in physiological pathways, which has the greatest potential to ameliorate unintended negative consequences. We suggest that these considerations allow an integrated pest management approach, with fewer negative ecological impacts and reduced likelihood of the evolution of resistant populations.

Conditional female strategies influence hatching success in a communally nesting iguana.

The decision of females to nest communally has important consequences for reproductive success. While often associated with reduced energetic expenditure, conspecific aggregations also expose females and offspring to conspecific aggression, exploitation, and infanticide. Intrasexual competition pressures are expected to favor the evolution of conditional strategies, which could be based on simple decision rules (i.e., availability of nesting sites and synchronicity with conspecifics) or on a focal individual's condition or status (i.e., body size). Oviparous reptiles that reproduce seasonally and provide limited to no postnatal care provide ideal systems for disentangling social factors that influence different female reproductive tactics from those present in offspring-rearing environments. In this study, we investigated whether nesting strategies in a West Indian rock iguana, Cyclura nubila caymanensis, vary conditionally with reproductive timing or body size, and evaluated consequences for nesting success. Nesting surveys were conducted on Little Cayman, Cayman Islands, British West Indies for four consecutive years. Use of high-density nesting sites was increasingly favored up to seasonal nesting activity peaks, after which nesting was generally restricted to low-density nesting areas. Although larger females were not more likely than smaller females to nest in high-density areas, larger females nested earlier and gained access to priority oviposition sites. Smaller females constructed nests later in the season, apparently foregoing investment in extended nest defense. Late-season nests were also constructed at shallower depths and exhibited shorter incubation periods. While nest depth and incubation length had significant effects on reproductive outcomes, so did local nest densities. Higher densities were associated with significant declines in hatching success, with up to 20% of egg-filled nests experiencing later intrusion by a conspecific. Despite these risks, nests in high-density areas were significantly more successful than elsewhere due to the benefits of greater chamber depths and longer incubation times. These results imply that communal nest sites convey honest signals of habitat quality, but that gaining and defending priority oviposition sites requires competitive ability.

Heterozygosity-Fitness Correlations Reveal Inbreeding Depression in Neonatal Body Size in a Critically Endangered Rock Iguana.

Inbreeding depression, though challenging to identify in nature, may play an important role in regulating the dynamics of small and isolated populations. Conversely, greater expression of genetic load can enhance opportunities for natural selection. Conditional expression concentrates these opportunities for selection and may lead to failure of detection. This study investigates the possibility for age-dependent expression of inbreeding depression in a critically endangered population of rock iguanas, Cyclura nubila caymanensis. We employ heterozygote-fitness correlations to examine the contributions of individual genetic factors to body size, a fitness-related trait. Nonsignificant reductions in homozygosity (up to 7%) were detected between neonates and individuals surviving past their first year, which may reflect natural absorption of inbreeding effects by this small, fecund population. The majority of variation in neonate body size was attributed to maternal or environmental effects (i.e., clutch identity and incubation length); however, heterozygosity across 22 microsatellite loci also contributed significantly and positively to model predictions. Conversely, effects of heterozygosity on fitness were not detectable when adults were examined, suggesting that inbreeding depression in body size may be age dependent in this taxon. Overall, these findings emphasize the importance of taking holistic, cross-generational approaches to genetic monitoring of endangered populations.