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Lipshutz, S. E.

Publications and source records attributed to Lipshutz, S. E..

10 recordsLinked to original sources

Habitat specialization structures population divergence and demographic variation in Amazonian floodplain birds

Understanding how species respond to environmental change requires linking ecological traits to gene flow and demographic history across dynamic landscapes. Using population genomic data from twelve co-distributed Amazonian riverine island birds, we show that habitat specialization predicts genetic structure, divergence, and effective population size. Species specialized on dynamic sandbar scrub habitats exhibit higher gene flow, and higher genetic diversity despite smaller effective population sizes. These patterns are consistent with dispersal tracking shifting resources, which decouples genetic diversity from population size. In contrast, river-edge forest specialists show stronger spatial genetic structure and lower genetic diversity despite larger populations, consistent with long-term isolation in more stable habitats. We also detect regional variation in effective population sizes and genetic diversity across Amazonian river sub-basins, potentially reflecting historical differences in floodplain habitat availability. Overall, our results highlight how non-equilibrium dynamics shape genomic variation and emphasize habitat-driven dispersal in diversification and persistence in seasonal systems.

evolutionary biology↗

Sex and breeding stage differences in neurogenomic profiles reflect hormone signaling in a socially polyandrous shorebird

In sex-role reversed species, females are socially polyandrous and compete for multiple mates, whereas males conduct the majority of parental care. To understand the extent to which physiological differences between females and males are shaped by sex roles, we examined sex differences in gene expression in sex-role reversed northern jacanas (Jacana spinosa). Given that females compete for mating opportunities, and males cycle between courtship and parental care, we predicted that transcriptomic profiles would be more similar between females and courting males, in contrast to female and parenting males. Leveraging a high quality de novo genome assembly, we conducted RNA-seq on two brain regions associated with the regulation of social behavior: the preoptic area of the hypothalamus and the nucleus taeniae. The majority of genes differentially expressed between the sexes were male-biased. Of these male-biased genes, the majority were located on the Z-chromosome. Contrary to our prediction, the greatest difference in autosomal gene expression was between females and courting males, in the preoptic area of the hypothalamus. Several differentially expressed genes related to elements of hormone signaling that are likely to be behaviorally salient, including higher expression of androgen receptor in females relative to parenting males, and higher expression of prolactin receptor in males, regardless of breeding stage. Some sex-associated gene networks were also associated with competitive traits, whereas others were associated with aggressive behaviors, regardless of sex. Few genes were differentially expressed between courting and parenting males, yet some nonetheless had connections to behavioral endocrinology, including prolactin, thyroid and insulin-like growth factor pathways. Our investigation of sex differences in gene expression can help to reveal the molecular mechanisms underlying female competition and male parental care in socially polyandrous species. We conclude that social polyandry is not a simple reversal in the direction of sex-biased gene expression in the brain, but rather a result of complex genetic and hormonal interactions that warrants further study.

genomics↗

Distinct networks of expressed genes are associated with neophobia in the hippocampus of male and female Eurasian tree sparrows (Passer montanus)

Neophobia, avoidance of novel stimuli, is an ecologically and evolutionarily relevant behavioral trait that varies among individuals and across species. Especially among wild animals, the neuromolecular mechanisms underlying individual variation in neophobia have not been well characterized. We examined three neophobic behaviors in captive female and male Eurasian tree sparrows (Passer montanus) from a wild population introduced to the USA in 1870: responses towards novel objects, novel foods, and repeated presentations of the same initially novel object. We compared transcriptomic patterns associated with neophobia in three brain regions, the striatum, dorsal hippocampus, and rostral hippocampus, using differential expression and co-expression network analyses. We found that the striatum and hippocampus had distinct transcriptomic profiles, as did the rostral and caudal subregions of the hippocampus, supporting recent hypotheses that these subregions are functionally specialized. Despite the absence of sex differences in neophobic behaviors, neophobia-associated gene modules revealed sex-specific patterns within brain regions. For females, neophobic behaviors more strongly correlated with gene modules in the caudal hippocampus, a region involved in stress and anxiety, whereas for males, neophobic behaviors correlated with gene modules in the rostral hippocampus, a region that may play a larger role in spatial cognition. These modules exhibited significant overlap, suggesting that neophobic behaviors in both females and males are driven by shared neurobiological mechanisms, though they exhibit sex-specific patterns of brain region localization. Further, this work highlights the importance of examining both male and female animals in neurobiological research.

animal behavior and cognition↗

How sex shapes transcriptome evolution in the songbird brain

Sex differences have long captivated scientists, yet the evolutionary rate of change in sex-biased gene expression has not been directly quantified. To address this issue, we introduce new options in CAGEE (Computational Analysis of Gene Expression Evolution), specifically unbounded Brownian motion and variable evolutionary rates among genes. We applied these features to brain transcriptomes of ten songbird species, half of which convergently evolved obligate cavity-nesting, an element of reproductive ecology linked to sex-specific changes in competitive behavior. We find that the degree of sex-bias - measured as male:female expression ratio for each gene - evolves twice as fast on the Z chromosome versus autosomes, but Z gene expression does not evolve at different rates among sexes. Most Z-linked genes are male-biased in their expression, but not all. These sex-balanced genes are not skewed in their rate of evolution, contrary to the hypothesis that some genes experience selection for balance and consequently evolve more slowly. Finally, the degree of sex-bias in gene expression evolves more quickly along obligate-cavity nesting lineages, suggesting that sex-specific selection may shape the evolution of brain sex differences, or lack thereof. Together, these results provide new insights into the interplay between sex and gene expression evolution.

evolutionary biology↗

Sexually selected traits predict female-biased philopatry in a sex-role reversed shorebird

Sex-biased dispersal plays a key role in shaping population dynamics and genetic structure. Two main hypotheses have been proposed for how territoriality and mating competition impact sex-biased dispersal. Female-biased dispersal is expected in monogamous systems with male resource defense, whereas male-biased dispersal is expected in polygynous systems with male competition over mates. However, patterns of sex-biased dispersal in polyandrous species, where females compete for both territories and mates, remain poorly understood. We investigated sex-biased dispersal in two polyandrous Jacana species, the Northern Jacana (Jacana spinosa) and Wattled Jacana (J. jacana), which exhibit intense female-female competition for territories and mates and differ in the strength of sexual selection. We analyzed sex-biased dispersal by assessing genetic differentiation and individual assignment indices in these jacana species across Central America. Our findings reveal strong male-biased dispersal in Northern Jacanas, indicated by higher genetic structuring and philopatry in females. In contrast, Wattled Jacanas showed no significant dispersal bias between sexes. Furthermore, sexually selected traits in Northern Jacana females, such as larger body mass, tarsus, and wing spur length, were associated with philopatry, suggesting that larger females retain territories, whereas smaller females disperse. To our knowledge, this is the first genetic evidence of male-biased dispersal in a polyandrous species. Our findings reveal that sexually selected traits, in addition to territorial and mate competition, are important for understanding species and sex differences in dispersal evolution.

evolutionary biology↗

Phylotranscriptomics reveals convergent behavioral evolution associated with shared and unique mechanisms in cavity-nesting songbirds

Uncovering the genomic bases of phenotypic adaptation is a major goal in biology, but this has been hard to achieve for complex behavioral traits. Here, we leverage the repeated, independent evolution of obligate cavity-nesting in birds to test the hypothesis that pressure to compete for a limited breeding resource has facilitated convergent evolution in behavior, hormones, and gene expression. We used an integrative approach, combining aggression assays in the field, testosterone measures, and transcriptome-wide analyses of the brain in wild-captured females and males. Our experimental design compared species pairs across five avian families, each including one obligate cavity-nesting species and a related species with a more flexible nest strategy. We find behavioral convergence, with higher levels of territorial aggression in obligate cavity-nesters, particularly among females. Across species, levels of testosterone in circulation were not associated with nest strategy, nor aggression. Phylogenetic analyses of individual genes and co-regulated gene networks revealed more shared patterns of brain gene expression than expected by drift, but the scope of convergent gene expression evolution was limited to a small percent of the genome. When comparing our results to other studies that did not use phylogenetic methods, we suggest that accounting for shared evolutionary history may reduce the number of genes inferred as convergently evolving. Altogether, we find that behavioral convergence in response to shared ecological pressures is associated with largely independent gene expression evolution across different avian families, punctuated by a narrow set of convergently evolving genes.

evolutionary biology↗

Comparative phylogeography reveals widespread cryptic diversity driven by ecology in Panamanian birds

Widespread species often harbor unrecognized genetic diversity, and investigating the factors associated with such cryptic variation can help us better understand the forces driving diversification. Here, we identify potential cryptic species based on a comprehensive dataset of COI mitochondrial DNA barcodes from 2,333 individual Panamanian birds across 429 species, representing 391 (59%) of the 659 resident landbird species of the country, as well as opportunistically sampled waterbirds. We complement this dataset with additional publicly available mitochondrial loci, such as ND2 and cytochrome b, obtained from whole mitochondrial genomes from 20 taxa. Using barcode identification numbers (BINs), we find putative cryptic species in 19% of landbird species, highlighting hidden diversity in the relatively well-described avifauna of Panama. Whereas some of these mitochondrial divergence events corresponded with recognized geographic features that likely isolated populations, such as the Cordillera Central highlands, the majority (74%) of lowland splits were between eastern and western populations. The timing of these splits are not temporally coincident across taxa, suggesting that historical events, such as the formation of the Isthmus of Panama and Pleistocene climatic cycles, were not the primary drivers of cryptic diversification. Rather, we observed that forest species, understory species, insectivores, and strongly territorial species--all traits associated with lower dispersal ability--were all more likely to have multiple BINs in Panama, suggesting strong ecological associations with cryptic divergence. Additionally, hand-wing index, a proxy for dispersal capability, was significantly lower in species with multiple BINs, indicating that dispersal ability plays an important role in generating diversity in Neotropical birds. Together, these results underscore the need for evolutionary studies of tropical bird communities to consider ecological factors along with geographic explanations, and that even in areas with well-known avifauna, avian diversity may be substantially underestimated. LAY SUMMARY- What factors are common among bird species with cryptic diversity in Panama? What role do geography, ecology, phylogeographic history, and other factors play in generating bird diversity? - 19% of widely-sampled bird species form two or more distinct DNA barcode clades, suggesting widespread unrecognized diversity. - Traits associated with reduced dispersal ability, such as use of forest understory, high territoriality, low hand-wing index, and insectivory, were more common in taxa with cryptic diversity. Filogeografia comparada revela amplia diversidad criptica causada por la ecologia en las aves de Panama RESUMENEspecies extendidas frecuentemente tiene diversidad genetica no reconocida, y investigando los factores asociados con esta variacion criptica puede ayudarnos a entender las fuerzas que impulsan la diversificacion. Aqui, identificamos especies cripticas potenciales basadas en un conjunto de datos de codigos de barras de ADN mitocondrial de 2,333 individuos de aves de Panama en 429 especies, representando 391 (59%) de las 659 especies de aves terrestres residentes del pais, ademas de algunas aves acuaticas muestreada de manera oportunista. Adicionalmente, complementamos estos datos con secuencias mitocondriales disponibles publicamente de otros loci, tal como ND2 o citocroma b, obtenidos de los genomas mitocondriales completos de 20 taxones. Utilizando los numeros de identificacion de codigo de barras (en ingles: BINs), un sistema taxonomico numerico que proporcina una estimacion imparcial de la diversidad potencial a nivel de especie, encontramos especies cripticas putativas en 19% de las especies de aves terrestres, lo que destaca la diversidad oculta en la avifauna bien descrita de Panama. Aunque algunos de estos eventos de divergencia conciden con caracteristicas geograficas que probablemente aislaron las poblaciones, la mayoria (74%) de la divergencia en las tierras bajas se encuentra entre las poblaciones orientales y occidentales. El tiempo de esta divergencia no coincidio entre los taxones, sugiriendo que eventos historicos tales como la formacion del Istmo de Panama y los ciclos climaticos del pleistoceno, no fueron los principales impulsores de la especiacion. En cambio, observamos asociaciones fuertes entre las caracteristicas ecologicas y la divergencia mitocondriale: las especies del bosque, sotobosque, con una dieta insectivora, y con territorialidad fuerte mostraton multiple BINs probables. Adicionalmente, el indice mano-ala, que esta asociado a la capacidad de dispersion, fue significativamente menor en las especies con BINs multiples, sugiriendo que la capacidad de dispersion tiene un rol importamente en la generacion de la diversidad de las aves neotropicales. Estos resultos demonstran la necesidad de que estudios evolutivos de las comunidades de aves tropicales consideren los factores ecologicos en conjunto con las explicaciones geograficos. Palabras clave: biodiversidad tropical, biogeografia, codigos de barras, dispersion, especies cripticas

evolutionary biology↗

Nesting strategy shapes territorial aggression but not testosterone: a comparative approach in female and male birds

Our understanding of the proximate and ultimate mechanisms shaping competitive phenotypes primarily stems from research on male-male competition for mates, even though female-female competition is also widespread. Obligate secondary cavity-nesting has evolved repeatedly across avian lineages, providing a useful comparative context to explore how competition over limited nest cavities shapes aggression and its underlying mechanisms across species. Although evidence from one or another cavity-nesting species suggests that territorial aggression is adaptive in both females and males, this has not yet been tested in a comparative framework. We tested the hypothesis that cavity-nesting generates more robust territorial aggression, in comparison to close relatives with less restrictive nesting strategies. Our focal species were two obligate secondary cavity-nesting species and two related species with more flexible nesting strategies in the same avian family: tree swallow (Tachycineta bicolor) vs. barn swallow (Hirundo rustica); Eastern bluebird (Sialia sialis) vs. American robin (Turdus migratorius). We assayed conspecific territorial aggression, and found that cavity-nesting species physically attacked a simulated intruder more often than their close relatives. This pattern held for both females and males. Because territorial aggression is often associated with elevated testosterone, we also hypothesized that cavity-nesting species would exhibit higher testosterone levels in circulation. However, cavity-nesting species did not have higher testosterone in circulation for either sex, despite some correlative evidence that testosterone is associated with higher rates of physical attack in female tree swallows. Our focus on a competitive context that is relevant to both sexes - competition over essential breeding resources - provides a useful comparative framework for co-consideration of proximate and ultimate drivers of reproductive competition in females and males.

animal behavior and cognition↗

Testosterone secretion varies in a sex- and stage-specific manner: insights on the regulation of competitive traits from a sex-role reversed species

Testosterone (T) mediates a variety of traits that function in competition for mates, including territorial aggression, ornaments, armaments, and gametogenesis. The link between T and mating competition has been studied mainly in males, but females also face selection pressures to compete for mates. Sex-role reversed species, in which females are the more competitive sex, provide a unique perspective on the role of T in promoting competitive traits. Here, we examine patterns of T secretion in sex-role reversed Northern Jacanas (Jacana spinosa) during breeding, when females are fertile and males are either seeking copulations or conducting parental care. We measured baseline levels of T in circulation along with a suite of behavioral and morphological traits putatively involved in mating competition. We evaluated hypotheses that levels of T track gonadal sex and parental role, and we begin to investigate whether T and competitive traits co-vary in a sex- and stage-specific manner. Although females had higher expression of competitive traits than males at either breeding stage, we found that females and incubating males had similar levels of T secretion, which were lower than those observed in copulating males. T was correlated with wing spur length in females and testes mass in copulating males, but was otherwise uncorrelated with other competitive traits. These findings suggest that levels of T in circulation alone do not predict variation in competitive traits across levels of analysis, including gonadal sex and parental role. Instead, our findings coupled with prior research indicate that selection for female mating competition and male care may generate different physiological regulation of competitive traits in jacanas. HighlightsO_LIIn role reversed species, females face stronger competition and males care for offspring C_LIO_LIWe examine testosterone (T) and competitive traits in female and male jacanas C_LIO_LICirculating T is similar in females and incubating males, but higher in copulating males C_LIO_LIBoth gonadal sex and parental role shape patterns of T secretion C_LIO_LIPhysiological regulation of competitive traits may differ in female and male jacanas C_LI

physiology↗

Species and sex divergence in vocalizations between hybridizing role-reversed shorebirds, Northern Jacana (Jacana spinosa) and Wattled Jacana (Jacana jacana)

Species-specific vocalizations can act as a reproductive isolating mechanism between closely related populations. We analyzed vocal divergence between two hybridizing species of sex-role reversed polyandrous shorebirds, the Northern Jacana (Jacana spinosa) and Wattled Jacana (Jacana jacana). We found that J. spinosa calls have higher peak frequency and fundamental frequency than J. jacana calls. We also compared calls between males and females, as both jacana species are sex-role reversed and females compete for male mates. Males produce calls with a higher peak frequency, exhibit shorter note lengths and emit a greater number of notes within a calling bout than females, which could relate to mate attraction. These results suggest that vocal divergence could act as a behavioral barrier to limit hybridization between the species and vocalizations may function differently between male and female jacanas.

animal behavior and cognition↗