Nocturnal behaviors that vary as a function of light intensity, either from the setting sun or the moon, are typically labeled as circadian or circalunar. Both of these terms refer to endogenous time-dependent behaviors. In contrast, the nightly reproductive and feeding behaviors of Vargula annecohenae, a bioluminescent ostracod (Arthropoda: Crustacea) fluctuate in response to light intensity, an exogenous factor that is not strictly time-dependent. We measured adult and juvenile activity of V. annecohenae throughout lunar cycles in January/February and June 2003. Overnight and nightly measurements of foraging and reproductive behavior of adult V. annecohenae indicated that activity was greatest when a critical "dark threshold" was reached and that the dark threshold for adult V. annecohenae is met when less than a third of the moon is visible or at the intensity of light 2-3 min before the start of nautical twilight when no moon is illuminated. Juvenile V. annecohenae were also nocturnally active but demonstrated little or no response to lunar illumination, remaining active even during brightly moonlit periods. In addition to light level, water velocity also influenced the behaviors of V. annecohenae, with fewer juveniles and adults actively foraging on nights when water velocity was high (>25 cm/s). Our data demonstrate that the strongest environmental factor influencing adult feeding and reproductive behaviors of V. annecohenae is the availability of time when illumination is below the critical dark threshold. This dependence on darkness for successful growth and reproduction allows us to classify darkness as a resource, in the same way that the term has been applied to time, space and temperature.
Mating behaviours are diverse and noteworthy, especially within species radiations where they may contribute to speciation. Studying how differences in mating behaviours arise between species can help us understand how diversity is generated at multiple biological levels. The bioluminescent courtship displays of cypridinid ostracods (or sea fireflies) are an excellent system for this because amazing variety evolves while using a conserved biochemical mechanism. We find that the evolution of one aspect in this behavioural phenotype-the duration of bioluminescent courtship pulses-is shaped by biochemical function. First, by measuring light production from induced bioluminescence in 38 species, we discovered differences between species in their biochemical reactions. Then, for 16 species for which biochemical, phylogenetic and behavioural data are all available, we used phylogenetic comparative models to show that differences in biochemical reaction are nonlinearly correlated with the duration of courtship pulses. This relationship indicates that changes to both enzyme (c-luciferase) function and usage have shaped the evolution of courtship displays, but that they differentially contribute to these phenotypic changes. This nonlinear dynamic may have consequences for the disparity of signalling phenotypes observed across species, and demonstrates how unappreciated diversity at the biochemical level can lead to inferences about behavioural evolution. BackgroundDisparate courtship behaviours are often a hallmark of species radiations [1-3], such that learning how differences evolve is critical to understanding the origins of biodiversity. Like other phenotypes, courtship displays are sensitive to natural selection, stochasticity, and historical and developmental constraints, with the interaction of these factors determining overall phenotype [4][5][6]. When predicting how such phenotypes evolve, it can be useful to build a theoretical space relating structure to function to better understand both realized and potential diversity; such 'phenospaces' give us insight into the evolutionary process. This has been particularly well used in functional morphology to describe how the evolution of biomechanical performance (a metric analogous to behavioural output) may be enabled [7] or constrained [8] due to differences in morphological traits. For example, in the courtship behaviours of woodpeckers, this approach has shown that morphological constraints in one aspect of the phenotype can be ameliorated by sexual selection acting to elaborate overall signal design in other ways [9]. However, behaviours are a non-additive output from many biological levels, not just morphology, and we might expect that variation in any one level can contribute to phenotypic evolution. Thus, given sufficient understanding of the relationship between structure
Understanding the genetic causes of evolutionary diversification is challenging because differences across species are complex, often involving many genes. However, cases where single or few genetic loci affect a trait that varies dramatically across a radiation of species provide tractable opportunities to understand the genetics of diversification. Here, we begin to explore how diversification of bioluminescent signals across species of cypridinid ostracods (“sea fireflies”) was influenced by evolution of a single gene, cypridinid‐luciferase. In addition to emission spectra (“colour”) of bioluminescence from 21 cypridinid species, we report 13 new c‐luciferase genes from de novo transcriptomes, including in vitro assays to confirm function of four of those genes. Our comparative analyses suggest some amino acid sites in c‐luciferase evolved under episodic diversifying selection and may be associated with changes in both enzyme kinetics and colour, two enzymatic functions that directly impact the phenotype of bioluminescent signals. The analyses also suggest multiple other amino acid positions in c‐luciferase evolved neutrally or under purifying selection, and may have impacted the variation of colour of bioluminescent signals across genera. Previous mutagenesis studies at candidate sites show epistatic interactions, which could constrain the evolution of c‐luciferase function. This work provides important steps toward understanding the genetic basis of diversification of behavioural signals across multiple species, suggesting different evolutionary processes act at different times during a radiation of species. These results set the stage for additional mutagenesis studies that could explicitly link selection, drift, and constraint to the evolution of phenotypic diversification.
Harmful algal blooms are occurring in large river ecosystems and at the mouth of large rivers with increasing frequency. In lentic systems, the chemical and physical conditions that promote harmful algal blooms are somewhat predictable but tracking prevalence and conditions that promote harmful algal blooms in lotic systems is much more difficult. We captured two of the most extreme discharge years within the last 20 years occurring in the Upper Mississippi River, allowing a natural experiment that evaluated how major shifts in discharge drive environmental variation and associated shifts in phytoplankton. Statistical models describing significant environmental covariates for phytoplankton assemblages and specific taxa were developed and used to identify management‐relevant numeric breakpoints at which environmental variables may promote the growth of specific phytoplankton and/or cyanobacteria. Our analyses supported that potentially toxin‐producing cyanobacteria dominate under high phosphorus concentration, low nitrogen concentration, low nitrogen‐to‐phosphorus ratio, low turbulence, low flushing, adequate light and warm temperatures. Cyanobacteria dominated in 2009 when low discharge and low flushing likely led to optimal growth environments for Dolichospermum, Aphanizomenon and Microcystis. Rarely will a single factor lead to the dominance, but multiple positive factors working in concert can lead to cyanobacteria proliferation in large rivers. Certain isolated backwaters with high phosphorus, low nitrogen, warm water temperatures and low potential for flushing could benefit from increased connection to channel inputs to reduce cyanobacterial dominance. Numerous examples of this type of habitat currently exist in the Upper Mississippi River and could benefit from reconnection to channel habitats.
Although the diversity, beauty, and intricacy of sexually selected courtship displays command the attention of evolutionists, the longevity of these traits in deep time is poorly understood. Population-based theory suggests sexual selection could either lower or raise extinction risk, resulting in high or low persistence of lineages with sexually selected traits. Furthermore, empirical studies that directly estimate longevity of sexually selected traits are uncommon. Sexually selected signals - including bioluminescent courtship - originated multiple times during evolution, allowing empirical study of their longevity after careful phylogenetic and divergence time analyses. Here, we estimate the first transcriptome-based molecular phylogeny and divergence times of Cypridinidae. We report extreme longevity of bioluminescent courtship, a trait important in mate choice and probably under sexual selection. Our relaxed-clock estimates of divergence times coupled with stochastic character mapping show luminous courtship evolved only once in Cypridinidae - in a Sub-Tribe we name Luxorina - at least 151 Million Years Ago (Ma) from cypridinid ancestors that used bioluminescence only in anti-predator displays, defining a Tribe we name Luminini. This time-calibrated molecular phylogeny of cypridinids will serve as a foundation for integrative and comparative studies on the biochemistry, molecular evolution, courtship, diversification, and ecology of cypridinid bioluminescence. The persistence of luminous courtship for hundreds of millions of years suggests that rates of speciation within the group exceeded extinction risk, which may contribute to the persistence of a diverse clade of signalling species and that sexual selection did not cause rapid loss of associated traits.
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