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Barrett, M., S. Schneider, P. Sachdeva, A. Gomez, S. Buchmann

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Barrett, M., S. Schneider, P. Sachdeva, A. Gomez, S. Buchmann Journal of Comparative Physiology A https://doi.org/10.1007/s00359-021-01492-4 ORIGINAL PAPER Neuroanatomical diferentiation associated with alternative reproductive tactics in male arid land bees, Centris pallida and Amegilla dawsoni Meghan Barrett1 · Sophi Schneider2 · Purnima Sachdeva1 · Angelina Gomez1 · Stephen Buchmann3,4 · Sean O’Donnell1,5 Received: 1 February 2021 / Revised: 19 May 2021 / Accepted: 22 May 2021 © The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021 Abstract Alternative reproductive tactics (ARTs) occur when there is categorical variation in the reproductive strategies of a sex within a population. These diferent behavioral phenotypes can expose animals to distinct cognitive challenges, which may be addressed through neuroanatomical diferentiation. The dramatic phenotypic plasticity underlying ARTs provides a powerful opportunity to study how intraspecifc nervous system variation can support distinct cognitive abilities. We hypothesized that conspecifc animals pursuing ARTs would exhibit dissimilar brain architecture. Dimorphic males of the bee species Centris pallida and Amegilla dawsoni use alternative mate location strategies that rely primarily on either olfaction (large-morph) or vision (small-morph) to fnd females. This variation in behavior led us to predict increased volumes of the brain regions supporting their primarily chemosensory or visual mate location strategies. Large-morph males relying mainly on olfaction had relatively larger antennal lobes and relatively smaller optic lobes than small-morph males relying primarily on visual cues. In both species, as relative volumes of the optic lobe increased, the relative volume of the antennal lobe decreased. In addition, A. dawsoni large males had relatively larger mushroom body lips, which process olfactory inputs. Our results suggest that the divergent behavioral strategies in ART systems can be associated with neuroanatomical diferentiation. Keywords Alternative mating tactics · Sensory diferentiation · Solitary bees Introduction insects, and include both behavioral and morphological trait variation (Shuster and Wade 2003; Paxton 2005; Oliveira Alternative reproductive tactics (ARTs) occur when there is et al. 2008; Shuster 2010). ARTs evolve when ftness gains categorical variation in the mating-related behaviors or traits can be achieved by pursuing divergent mating strategies, of same-sex individuals within a population (Oliveira et al. leading to selection on phenotypes that maximize the suc- 2008). ARTs have evolved in diverse animal taxa, including cess of two or more specialized morphs (Shuster 2010). fsh, crustaceans, birds, amphibians/reptiles, mammals, and Because morphs often develop via phenotypic plasticity, ARTs allow for the study of behavioral and morphological * variation within a population that are not dependent upon Meghan Barrett genotypic diferences (Kukuk 1996; reviewed in Oliveira [email protected] et al. 2008). In this way, ARTs provide a unique and pow- 1 Department of Biology, Drexel University, Philadelphia, PA, erful opportunity to explore the evolution of relationships USA between behavioral and morphological specialization. 2 Upper Dublin, PA, USA Neuroecology theory predicts that relative investment in 3 Department of Entomology, University of Arizona, Tucson, functionally discrete regions of the brain will be correlated AZ, USA to the cognitive demands of an organism’s environment/ 4 Department of Ecology and Evolutionary Biology, University behaviors, due to constraints imposed by the high meta- of Arizona, Tucson, AZ, USA bolic cost of producing and maintaining neural tissue (Aiello 5 Department of Biodiversity, Earth, and Environmental and Wheeler 1995; Sherry 2006; Liao et al. 2016; Niven Science, Drexel University, Philadelphia, PA, USA 2016; Luo et al. 2017). Energy limitation thus places neural Vol.:(0123456789)1 3 Journal of Comparative Physiology A systems under selective pressure for optimal investment chase after females ‘upwind’ of them, as males are oriented (Niven and Laughlin 2008). Because successful mate loca- 360° around the vegetation—not just on the downwind side— tion behaviors are expected to be strongly linked to repro- and always orient facing the largest open area visually, away ductive success, diferent sensory mate location strategies from the vegetation and not necessarily into the wind (Barrett, could be associated with neuroanatomical diferentiation in personal observation). the regions of the brain that support those sensory systems. Similarly, the large ‘majors’ of A. dawsoni exhibit a fxed We hypothesized that conspecifc animals utilizing ARTs strategy, patrolling female emergence sites and likely using would have diferent brain architecture patterns, related cuticular hydrocarbon cues to locate females waiting within to the cognitive demands of their morph-specifc mating emergence tunnels, before fghting other males and/or guard- behaviors. ing potential mates (Alcock 1997; Simmons et al. 2003). The male morphs of Centris pallida Fox, found in the Smaller A. dawsoni ‘minor’ males rarely patrol emergence Sonoran Desert of the USA and Northern Mexico, and sites, instead typically hovering or patrolling near blooming Amegilla dawsoni Rayment (Dawson’s burrowing bee), host plant vegetation and use visual cues to locate females found in the deserts of Western Australia, use alternative (Houston 1991; Alcock 1997). sensory mate location strategies. In C. pallida, large-morph In summary, the large-morph males (e.g. metanders or males are morphologically distinct based on coloration and majors) of both species are behaviorally fxed on using chem- hind leg morphology (called ‘metanders’ with ‘swollen’ legs osensory cues to locate females (Alcock et al. 1977; Alcock in Snelling 1984 or ‘largest males’ in Alcock et al. 1977). 1997; Simmons et al. 2003), while the small-morph males are These males have a fxed mate location strategy, using che- more behaviorally fexible but rely more heavily on visual cues mosensory cues to patrol close to the soil surface in search to locate mates when hovering. We predicted brain structure for females buried underground. Males land near buried would difer between the male morphs in both species, with females and repetitively touch the soil with their antennae relative increases in tissue investment in brain regions that (typical insect odor-tracking behavior on a surface; Wenner support mating-tactic relevant cognitive abilities. 1974), before digging up the buried female (Alcock et al. We analyzed whether relative brain investment patterns 1977). Chemosensory cues are both sufcient and neces- difered between the morphs of each species in their anten- sary for locating females–males will dig up dead, buried nal lobes (AL), which receive chemosensory information females that are not moving or visible but will not dig up from the antennae, and their optic lobes (OL), which receive vibrating objects (Alcock et al. 1976). Other males will fght visual information from the eyes (Kenyon 1896). We tested with the digging male for the opportunity to mate with the for a negative correlation in investment between visual and emerging females, with the largest male typically winning olfactory brain regions, which are seen in comparative stud- and copulating with the female (Alcock 1976, 2013; Alcock ies of other insects (often described as trade-ofs: Niven et al. 1976, 1977). and Laughlin 2008, Stöckl et al. 2016; Kessey et al. 2019; In contrast to the fxed mate location strategy the large-male Özer and Carle 2020). In addition to analyzing investment morph uses, small-morph males can be behaviorally fexible. in peripheral sensory brain regions, we asked whether the They may patrol the ground like large-morph males or alter- relative volumes of the mushroom body (MB) calyces (we natively hover near vegetation, chasing after and mating with analyzed the lip and collar separately) difered between any females or mating pairs they locate visually (Alcock 1976, the morphs. The mushroom bodies are involved in learn- 1979, 1984; Alcock et al. 1977). Visual cues are likely the only ing, memory, and sensory integration, and receive olfactory or primary sensory strategy used while hovering. First, hover- input to the MB calyx lip and visual input to the MB calyx ing males chase any insect passing through their visual feld collar (Fahrbach 2006; Paulk and Gronenberg 2008). We (even those several meters away, C. pallida males, and non-C. thus predicted that the large-morph males that are fxed on pallida insects). Second, males only chase nearby hovering chemosensory cues for mate location would have relatively males when they enter their visual feld, even though they are larger MB lips and ALs, and relatively smaller MB collars often hovering less than a meter away for several hours. If and OLs, as compared with the small-morph males that rely olfaction were in use, males would detect, orient towards, and more heavily on vision but are behaviorally fexible. chase after nearby males even when not in their visual feld (e.g. drones of Apis mellifera, Brandstaetter et al. 2014). Third, male C. pallida do not discriminate between the odors of male Materials and methods or female C. pallida (when digging Alcock et al. 1976; and even in close contact, Alcock and Buchmann 1985), making it Specimen collection unlikely that they are tracking the odor of a single, fast-moving female bee in the midst of a turbulent aggregation of thousands
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