The selection of animal signal form often changes significantly with the environment, yet signal form may be environment-dependent. Little is known about how variation in individual responses to changing environments affects the relationship between selection and the subsequent evolution of signal traits. To address this question, we assess the effects of variation in temperature on individual signaling and mating behavior responses across temperatures in the wolf spider Schizocosa floridana. By running repeated-measures trials, we find that temperature has predictable effects on signal form, but that the performance of individual courters is not consistent across temperatures. Traits associated with courtship rate generally increase at higher temperatures but inter-individual consistency in response to temperature change is low, despite consistent female preferences for increased courtship rate at all temperatures. Interestingly, the production of the likely most recently evolved signal component, the chirp, is consistent within signalers and predicts male performance across temperatures. Despite this, female preferences for chirp duration appear only at higher temperatures. Taken together, our results suggest that individual courter responses to changing temperatures have the potential to dampen or eliminate patterns of selection that are evident across temperatures. We discuss these results in light of current research on mating behavior and sexual selection.
Heterospecific interactions between nascent species offer insights into how sexual selection shapes novel traits, illuminating patterns in species interactions and diversification. We tested female preferences between two recently diverged, allopatric species of jumping spiders: Habronattus americanus PLC, with red-coloured males performing short multimodal displays, and Habronattus sansoni CC, with brown-coloured males performing long multimodal displays. Mate choice experiments showed that females of both species preferred H. americanus PLC males. To examine the role of red coloration, we manipulated male coloration in both species. Results indicated that red-painted H. sansoni CC males experienced an increase in mating success, whereas brown-painted H. americanus PLC males did not show reduced success. Our study suggests that (i) strong latent female preferences can drive unidirectional introgression across species boundaries, potentially leading to genomic homogenization; (ii) latent preferences may override preferences for existing traits; and (iii) the geographical distribution of colour morphs is consistent with a hypothesis of strong latent preferences across populations. Overall, our study demonstrates the role that mating interactions can play in speciation dynamics.
Substrate-borne vibrations are ubiquitous in nature and are used by diverse taxa to communicate and to obtain information about their environments. However, substrate-borne vibrations remain understudied compared with other sensory and signaling modalities, in part due to human sensory biases. In addition, understanding and quantifying the transmission of vibrations remains a challenging task due to it being dependent on both signal properties and properties of the substrates that the signals transmit through. Here, we provide methods for playing back and measuring the transmission of vibrations throughout a substrate. Using linear resonant actuators, we conducted playbacks of pure tones and frequency sweeps on wooden dowels and on the stems of potted Ptelea trifoliata L. (Rutaceae) plants. We used scanning laser Doppler vibrometry to measure the signals at multiple locations along the length of the dowels and plant stems. We demonstrate that playback of a frequency sweep yields more data in a shorter amount of time than multiple playbacks and measurements of pure tone signals. Our results are also consistent with previous findings showing that signals produce frequency and location specific minima and maxima (nodes and antinodes) throughout the substrates, rather than simply attenuating with distance. This results in filtering of signals, such that their spectra are unique at any given measurement location-illustrating the importance of measuring vibrations at multiple locations. We discuss the implications of such filtering phenomena for vibrationally signaling animals and the biotremologists that study them.
Sexual selection is an important evolutionary force and despite extensive research, understanding mate choice on naturally occurring trait variation remains an intriguing area of study. The correlation between mass, a trait associated with courter viability and common target for mate choice, and signals is particularly noteworthy. This study focuses on Schizocosa mccooki, the largest member of a wolf spider genus renowned for its diverse complex male courtship. Our objective was to understand the relationship of male mass and other courtship signals on female choice within this species. We conducted lab experiments involving random pairings of field caught males and females, recording vibratory courtship and its outcomes. Our findings revealed that S. mccooki courtship consisted of vibratory signals with two major components, thumps and raps. Male mass, overall courtship vigor, and thump duration were found to predict mating success. Interestingly, we found no correlation between temporal traits and mass suggesting independent information and an absence of trade-offs between mass, courtship vigor, and signal component rates/durations. Instead, we found that heavier males tend to produce thumps with lower frequencies. The finding that male mass predicts mating success contrasts with patterns observed in other species in this well-studied genus. By uncovering the mate choice patterns of S. mccooki, this study underscores the importance of comparative studies to understand the ways in which sexual selection drives diversification, even among closely related taxa.
Defensive strategies, like other life-history traits favored by natural selection, may pose constraints on reproduction. A common anti-predator defense strategy that increases immediate survival is autotomy—the voluntary release of body parts. This type of morphological damage is considered to impose future costs for reproduction and fitness. We tested an alternative hypothesis that animals are robust (able to withstand and overcome perturbations) to this type of damage and do not experience any fitness costs in reproductive contexts. We explored the effects of experimental leg loss on the reproductive behavior of one species of Neotropical Prionostemma harvestmen. These arachnids undergo autotomy frequently, do not regenerate legs, and their courtship and mating necessitate the use of legs. We assessed the effect of losing different types of legs (locomotor or sensory) on courtship behavior and mating success in males. We found no differences in the mating success or in any measured aspect of reproductive behavior between eight-legged males and males that experienced loss of legs of any type. Additionally, we found that morphological traits related to body size did not predict mating success. Overall, our experimental findings support the null hypothesis that harvestmen are robust to the consequences of morphological damage and natural selection favors strategies that increase robustness. Significance statement In order to survive encounters with predators, animals have evolved many defensive strategies. Some of those behaviors, however, can come with a cost to their overall body condition. For example, some animals can voluntarily lose body parts (tails, legs, etc.) to escape. This process can then affect many aspects of an animal’s life, including reproduction. In a group of harvestmen (daddy long-legs) from Costa Rica, we tested the hypothesis that males are robust to the potential consequences of losing legs, and will not experience costs. We found that males that lost either legs used for locomotion or for sensory perception reproduced in the same way as animals with all of their legs. Consequently, we demonstrate that these arachnids are able to withstand the loss of legs with no effects on reproduction.
In animal taxa, the behavior of choosing a microhabitat determines the context in which individuals engage in all other behaviors and interactions. Microhabitat choice has particularly important implications for animal communication, because the successful transmission of information between individuals is highly context-dependent. Substrate-borne vibrations, which are commonly produced, detected, and used for communication by arthropods, are especially influenced by substrate choice because substrates vary widely in their vibration transmission properties. In this laboratory-based study, we examine vibration transmission properties of substrates commonly encountered in nature by the jumping spider Habronattus clypeatus and also examine whether these spiders exhibit a preference for particular substrates using a choice experiment. We predicted that spiders would prefer substrates that can better transmit vibratory signals. We found that leaf litter minimized the attenuation of vibratory signals, while rocks and sand sharply attenuated the signals. In behavioral trials, more spiders chose leaf litter or rocks as their first substrate over sand. Further, spiders spent more time on, and were more likely to jump to, leaf litter and rocks than sand. These results suggest that substrate preference by H. clypeatus partially matches the choice that would maximize signal transmission efficiency, indicating that the ability to communicate with conspecifics may influence these animals' choice of microhabitat.
EDITORIAL article Front. Ecol. Evol., 05 November 2021Sec. Behavioral and Evolutionary Ecology https://doi.org/10.3389/fevo.2021.788711
Jumping in animals presents an interesting locomotory strategy as it requires the generation of large forces and accurate timing. Jumping in arachnids is further complicated by their semi-hydraulic locomotion system. Among arachnids, jumping spiders (Family Salticidae) are agile and dexterous jumpers. However, less is known about jumping in small salticid species. Here we used Habronattus conjunctus, a small jumping spider (body length ~ 4.5 mm) to examine its jumping performance and compare it to that of other jumping spiders and insects. We also explored how legs are used during the takeoff phase of jumps. Jumps were staged between two raised platforms. We analyzed jumping videos with DeepLabCut to track 21 points on the cephalothorax, abdomen, and legs. By analyzing leg liftoff and extension patterns, we found evidence that H. conjunctus primarily uses the third legs to power jumps. We also found that H. conjunctus jumps achieve lower takeoff speeds and accelerations than most other jumping arthropods, including other jumping spiders. Habronattus conjunctus takeoff time was similar to other jumping arthropods of the same body mass. We discuss the mechanical benefits and drawbacks of a semi-hydraulic system of locomotion and consider how small spiders may extract dexterous jumps from this locomotor system.
Synopsis To capture prey otherwise unattainable by muscle function alone, some animal lineages have evolved movements that are driven by stored elastic energy, producing movements of remarkable speed and force. One such example that has evolved multiple times is a trap-jaw mechanism, in which the mouthparts of an animal are loaded with energy as they open to a wide gape and then, when triggered to close, produce a terrific force. Within the spiders (Araneae), this type of attack has thus far solely been documented in the palpimanoid family Mecysmaucheniidae but a similar morphology has also been observed in the distantly related araneoid subfamily Pararchaeinae, leading to speculation of a trap-jaw attack in that lineage as well. Here, using high-speed videography, we test whether cheliceral strike power output suggests elastic-driven movements in the pararchaeine Pararchaea alba. The strike speed attained places P. alba as a moderately fast striker exceeding the slowest mecysmaucheniids, but failing to the reach the most extreme high-speed strikers that have elastic-driven mechanisms. Using microcomputed tomography, we compare the morphology of P. alba chelicerae in the resting and open positions, and their related musculature, and based on results propose a mechanism for cheliceral strike function that includes a torque reversal latching mechanism. Similar to the distantly related trap-jaw mecysmaucheniid spiders, the unusual prosoma morphology in P. alba seemingly allows for highly maneuverable chelicerae with a much wider gape than typical spiders, suggesting that increasingly maneuverable joints coupled with a latching mechanism may serve as a precursor to elastic-driven movements.
The diversity of signalling traits within and across taxa is vast and striking, prompting us to consider how novelty evolves in the context of animal communication. Sexual selection contributes to diversification, and here we endeavour to understand the initial conditions that facilitate the maintenance or elimination of new sexual signals and receiver features. New sender and receiver variants can occur through mutation, plasticity, hybridization and cultural innovation, and the initial conditions of the sender, the receiver and the environment then dictate whether a novel cue becomes a signal. New features may arise in the sender, the receiver or both simultaneously. We contend that it may be easier than assumed to evolve new sexual signals because sexual signals may be arbitrary, sexual conflict is common and receivers are capable of perceiving much more of the world than just existing sexual signals. Additionally, changes in the signalling environment can approximate both signal and receiver changes through a change in transmission characteristics of a given environment or the use of new environments. The Anthropocene has led to wide-scale disruption of the environment and may thus generate opportunity to directly observe the evolution of new signals to address questions that are beyond the reach of phylogenetic approaches.
It is not uncommon to find courtship displays that incorporate numerous components across different sensory modalities. We studied displays in male jumping spiders of the genus Habronattus F.O. Pickard-Cambridge, 1901, which court females using a combination of ornament and motion (dance) displays coordinated with vibrational songs. To explore the diversity in Habronattus courtship complexity, we focused on quantifying the dance and vibratory displays in nine members of the Habronattus clypeatus species group, with preliminary observations on two additional species from this group. Additionally, we looked at display variation across populations in two widespread species from this group. We document three main courtship types: "stilting'', "buzzing'', and "spinning'', each identifiable by the presence or emphasis on particular display types. We found that for the widespread species H. clypeatus (Banks, 1895), different populations differed significantly and could be classified as either stilting or buzzing types. We discuss these results in relation to broader patterns of signal evolution and diversification in Habronattus.
Because habitats present different costs and benefits in contexts ranging from foraging to mating to predator avoidance, decisions about habitat use likely involve significant trade-offs across behavioural contexts. We examine this possibility in Schizocosa floridana, a cursorial wolf spider whose habitat consists of multiple substrates, including oak and pine litter, and sand. However, S. floridana restricts its use of habitat to oak litter. Substrate environments vary significantly in the degree to which they transmit visual and vibratory information. Previous work found that oak litter best transmits the substrate-borne vibrations that are critical to mating communication. However, oak litter may reduce the availability of visual information, which is known to be important for prey capture in other wolf spider species. Here, we test the relationship between substrate and prey capture efficiency in S. floridana. We examine substrate use in a foraging context via two laboratory-based experiments to (1) assess differences in prey capture efficiency among the three most common substrates in the field and to (2) determine which sensory modalities are involved in prey capture. We found that prey capture rates were highest on sand despite the fact that sand is the least used substrate by S. floridana in the wild. We also found no conclusive evidence that either the visual or the vibratory sensory modalities are critical for prey capture. Our results thus suggest that strict habitat specialization such as that exhibited by S. floridana is beneficial in some ecological contexts but costly in others. (c) 2021 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
For many animals, early life stages are at higher risk of mortality from sources like predation, disease, and environmental fluctuations than other life stages (Clutton-Brock, 2001). To increase their reproductive success, some parents invest time and energy into protecting offspring by building protective structures. Benefits of protective structures like nests have been found across species. For example, nests increase reproductive success for many mammals (Reichman & Smith, 1990), birds (Mainwaring et al., 2014), reptiles (Angilletta et al., 2009), fish (Ishimatsu et al., 2007; Takegaki & Nakazono, 2000), and arthropods (Hieber, 1992b; Wyatt, 1986). However, the benefits of nests are unlikely to be static through time. From the day they are constructed, conditions outside of nest like environmental conditions and predator dynamics are constantly fluctuating and threatening to damage the nest and/or harm offspring. The dynamic nature of nest benefits through time has great implications for how much parents invest in building and/or Received: 15 July 2020 | Revised: 2 December 2020 | Accepted: 4 December 2020 DOI: 10.1111/eth.13120
AbstractFinding shelter and surviving encounters with predators are pervasive challenges for animals. These challenges may be exacerbated after individuals experience bodily damage. Certain forms of damage arise voluntarily in animals; for instance, some taxa release appendages (tails, legs, or other body parts) as a defensive strategy (“autotomy”). This behavior, however, may pose long‐term negative consequences for habitat use and survival. Additionally, these putative consequences are expected to vary according to the function of the lost body part. We tested the effects of losing different functional leg types (locomotor or sensory) on future habitat use and survival in a Neotropical species of Prionostemma harvestmen (Arachnida: Opiliones) that undergo frequent autotomy but do not regrow limbs. Daytime surveys revealed that both eight‐legged harvestmen and harvestmen missing legs roosted in similar frequencies across habitats (tree bark, mossy tree, or fern), and perched at similar heights. Mark–recapture data showed that harvestmen that lost sensory legs roosted in tree bark less frequently, but on mossy trees more frequently. On the contrary, we did not observe changes in habitat use for eight‐legged animals or animals that lost locomotor legs. This change might be related to sensory exploration and navigation. Lastly, we found that recapture rates across substrates were not affected by the type of legs lost, suggesting that leg loss does not impact survival. This potential lack of effect might play a role in why a defensive strategy like autotomy is so prevalent in harvestmen despite the lack of regeneration.
Animals communicate using a diversity of signals produced by a wide array of physical structures. Determining how a signal is produced provides key insights into signal evolution. Here, we examine a complex vibratory mating display produced by male Schizocosa floridana wolf spiders. This display contains three discrete substrate-borne acoustic components (known as "thumps", "taps", and "chirps"), each of which is anecdotally associated with the movement of a different body part (the pedipalps, legs, and abdomen respectively). In order to determine the method of production, we employ a combination of high-speed video/audio recordings and SEM imaging of possible sound-producing structures. Previous work has suggested that the "chirp" component is tonal, a signal trait that would be potentially unique in the genus. We measured signal tonality for all courtship components, as well as for courtship components from sixteen other Schizocosa wolf spiders. Our results suggest that S. floridana produces courtship song using a combination of shared (palpal stridulation and foreleg percussion) and novel (abdominal movement) sound production mechanisms. Of particular interest, the "chirp", which is produced using a novel abdominal production mechanism, is the only known tonal signal with acoustic properties that are unique within the genus. We argue that the potential evolution of a novel sound production mechanism has opened up a new axis of signaling trait space in this species, with important implications for how this signal is likely to function and evolve.
Understanding diversity has been a pursuit in evolutionary biology since its inception. A challenge arises when sexual selection has played a role in diversification. Questions of what constitutes a 'species', homoplasy vs. synapomorphy, and whether sexually selected traits show phylogenetic signal have hampered work on many systems. Peacock spiders are famous for sexually selected male courtship dances and peacock-like abdominal ornamentation. This lineage of jumping spiders currently includes over 90 species classified into two genera, Maratus and Saratus. Most Maratus species have been placed into groups based on secondary sexual characters, but evolutionary relationships remain unresolved. Here we assess relationships in peacock spiders using phylogenomic data (ultraconserved elements and RAD-sequencing). Analyses reveal that Maratus and the related genus Saitis are paraphyletic. Many, but not all, morphological groups within a 'core Maratus' lade are recovered as genetic clades but we find evidence for undocumented speciation. Based on original observations of male courtship, our comparative analyses suggest that courtship behaviour and peacock-like abdominal ornamentation have evolved sequentially, with some traits inherited from ancestors and others evolving repeatedly and independently from 'simple' forms. Our results have important implications for the taxonomy of these spiders, and provide a much-needed evolutionary framework for comparative studies of the evolution of sexual signal characters.
Animals have evolved adaptations to deal with environmental challenges. For instance, voluntarily releasing appendages (autotomy) to escape potential predators. Although it may enhance immediate survival, this self-imposed bodily damage may convey long-term consequences. Hence, compensatory strategies for this type of damage might exist. We experimentally induced autotomy in Prionostemma harvestmen. These arachnids are ideal to examine this topic because they show high levels of leg loss in the field but do not regenerate their legs. We video-recorded animals moving on a horizontal track and reconstructed their 3D trajectories with custom software tools to measure locomotor performance. Individuals that lost either three legs total or two legs on the same side of the body showed an immediate and substantial decrease in velocity and acceleration. Surprisingly, harvestmen recovered initial performance after 2 days. This is the quickest locomotor recovery recorded for autotomizing animals. We also found post-autotomy changes in stride and postural kinematics, suggesting a role for kinematic adjustments in recovery. Additionally, following leg loss, some animals changed the gaits used during escape maneuvers, and/or recruited the ‘sensory’ legs for locomotion. Together, these findings suggest that harvestmen are mechanically robust to the bodily damage imposed by leg loss.
Environmental context is a crucial factor that influences sexual communication systems. Particularly in ectotherms, which cannot metabolically regulate their body temperature, temperature has an outsized effect on these intraspecific interactions. Using the desert-dwelling jumping spider Habronattus clypeatus, we assessed how temperature impacts various parts of the male signal and female mate choice for the signal. These spiders have multimodal, temporally structured courtship displays that begin with visual-only ‘sidling’ displays and proceed to multimodal visual and vibratory displays. To examine temperature effects, we performed sequential choice mating experiments (N=45 trials) at two temperature treatments: hot (∼50°C) and room temperature (∼25°C). We found first that variation in the different stages of courtship segregated onto different principal components. The only aspect of male courtship that females expressed preference for was sidling courtship, but only at the higher temperature. Females also preferred to mate with heavier males at all temperatures. Specifically, females preferred to mate with males that performed shorter sidling displays. This is reflected by shorter copulation times in the warm treatment as well. We also found that temperature impacted only vibratory courtship and not sidling courtship. Our results highlight the importance of understanding environmental context in studies of animal communication. We also stress how a holistic, rather than reductive, approach to complex communication systems is vital in order to understand how selection acts upon them.
Temperature is known to influence many aspects of organisms and is frequently linked to geographical species distributions. Despite the importance of a broad understanding of an animal's thermal biology, few studies incorporate more than one metric of thermal biology. Here we examined an elevational assemblage of Habronattus jumping spiders to measure different aspects of their thermal biology including thermal limits (CTmin, CTmax), thermal preference, (V)over dotCO(2) as proxy for metabolic rate, locomotor behavior and warming tolerance. We used these data to test whether thermal biology helped explain how species were distributed across elevation. Habronattus had high CTmax values, which did not differ among species across the elevational gradient. The highest-elevation species had a lower CTmin than any other species. All species had a strong thermal preference around 37 degrees C. With respect to performance, one of the middle elevation species was significantly less temperature-sensitive in metabolic rate. Differences between species with respect to locomotion (jump distance) were likely driven by differences in mass, with no differences in thermal performance across elevation. We suggest that Habronattus distributions follow Brett's rule, a rule that predicts more geographical variation in cold tolerance than heat. Additionally, we suggest that physiological tolerances interact with biotic factors, particularly those related to courtship and mate choice to influence species distributions. Habronattus also had very high warming tolerance values (> 20 degrees C, on average). Taken together, these data suggest that Habronattus are resilient in the face of climate-change related shifts in temperature.