skip to main content


Title: Reproductive biology of harvestmen (Arachnida: Opiliones): a review of a rapidly evolving research field
Abstract

Harvestmen are a major arachnid order that has experienced a dramatic increase in biological knowledge in the 21st century. The publication of the book Harvestmen: The Biology of Opiliones in 2007 stimulated the development of many behavioral studies. Although the book is relatively recent, our understanding of the reproductive biology of harvestmen is already outdated due to the fast accumulation of new data. Our goal is to provide an updated review of the subject to serve as a benchmark for the following years. In the pre-copulatory phase, we explore the evolution of facultative parthenogenesis, the factors that may affect the types of mating system, and the role of nuptial gifts in courtship. Regarding the copulatory phase, harvestmen are unique arachnids because they have aflagellate spermatozoa and a penis with complex morphology. We discuss the implications of these two features for sperm competition and cryptic female choice. In the post-copulatory phase, we connect oviposition site selection and climate conditions to the widespread occurrence of resource defense polygyny, alternative reproductive tactics, and sexual dimorphism in several clades of tropical harvestmen. Finally, we present the different forms of parental care in the order, and discuss the benefits and costs of this behavior, which can be performed either by females or males. Throughout the review, we indicate gaps in our knowledge and subjects that deserve further studies. Hopefully, the information synthesized here will stimulate researchers worldwide to embrace harvestmen as a study system and to improve our effort to unravel the mysteries of their reproductive biology.

 
more » « less
NSF-PAR ID:
10403871
Author(s) / Creator(s):
; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Current Zoology
ISSN:
1674-5507
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The field of comparative ageing biology has greatly expanded in the past 20 years. Longitudinal studies of populations of reptiles with a range of maximum lifespans have accumulated and been analysed for evidence of mortality senescence and reproductive decline. While not as well represented in studies of amniote senescence, reptiles have been the subjects of many recent demographic and mechanistic studies of the biology of ageing.

    We review recent literature on reptile demographic senescence, mechanisms of senescence, and identify unanswered questions. Given the ecophysiological and demographic diversity of reptiles, what is the expected range of reptile senescence rates? Are known mechanisms of ageing in reptiles consistent with canonical hallmarks of ageing in model systems? What are the knowledge gaps in our understanding of reptile ageing?

    We find ample evidence of increasing mortality with advancing age in many reptiles. Testudines stand out as slower ageing than other orders, but data on crocodilians and tuatara are sparse. Sex‐specific analyses are generally not available. Studies of female reproduction suggest that reptiles are less likely to have reproductive decline with advancing age than mammals.

    Reptiles share many physiological and molecular pathways of ageing with mammals, birds and laboratory model organisms. Adaptations related to stress physiology coupled with reptilian ectothermy suggest novel comparisons and contrasts that can be made with canonical ageing phenotypes in mammals. These include stem cell and regeneration biology, homeostatic mechanisms, IIS/TOR signalling, and DNA repair.

    To overcome challenges to the study of reptile ageing, we recommend extending and expanding long‐term monitoring of reptile populations, developing reptile cell lines to aid cellular biology, conducting more comparative studies of reptile morphology and physiology sampled along relevant life‐history axes and sequencing more reptile genomes for comparative genomics. Given the diversity of reptile life histories and adaptations, achieving these directives will likely greatly benefit all ageing biology.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
    more » « less
  2. Abstract

    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 NeotropicalPrionostemmaharvestmen. 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.

     
    more » « less
  3. Abstract

    Heterospecific mating frequency is critical to hybrid zone dynamics and can directly impact the strength of reproductive barriers and patterns of introgression. The effectiveness of post‐mating prezygotic (PMPZ) reproductive barriers, which include reduced fecundity via heterospecific matings and conspecific sperm precedence, may depend on the number, identity and order of mates. Studies ofPMPZbarriers suggest that they may be important in many systems, but whether these barriers are effective at realistic heterospecific mating frequencies has not been tested. Here, we evaluate the strength of cryptic reproductive isolation in two leaf beetles (Chrysochus auratusandC. cobaltinus) in the context of a range of heterospecific mating frequencies observed in natural populations. We found both species benefited from multiple matings, but the benefits were greater inC. cobaltinusand extended to heterospecific matings. We found thatPMPZbarriers greatly limited hybrid production byC. auratusfemales with moderate heterospecific mating frequencies, but that their effectiveness diminished at higher heterospecific mating frequencies. In contrast, there was no evidence forPMPZbarriers inC. cobaltinusfemales at any heterospecific mating frequency. We show that integrating realistic estimates of cryptic isolation with information on relative abundance and heterospecific mating frequency in the field substantially improves our understanding of the strong directional bias in F1 production previously documented in theChrysochushybrid zone. Our results demonstrate that heterospecific mating frequency is critical to understanding the impact of cryptic post‐copulatory barriers on hybrid zone structure and dynamics, and that future studies of such barriers should incorporate field‐relevant heterospecific mating frequencies.

     
    more » « less
  4. Abstract

    In this study, we explored the potential contribution of the gut microbiome to reproductive isolation in tunnelling dung beetles, usingOnthophagus taurus(Schreber, 1759) and its sister speciesO. illyricus(Scopoli, 1763) as a model system (Coleoptera: Scarabaeidae: Scarabaeinae: Onthophagini). Gut microbiota play critical roles in normative development of these beetles, and are vertically inherited via a maternally derived faecal pellet called thepedestal. We first compared the developmental outcomes of individuals reared with pedestals derived from either the same or the sister species (SelfandCrossinoculation treatments, respectively). We then crossed the resulting adultO. taurusin three combinations (Selffemale XSelfmale;Selffemale XCrossmale;Crossfemale XSelfmale). We predicted that if the vertically transmitted gut microbiome plays a role in reproductive isolation by facilitating species recognition, theSelfXSelfline would have improved reproductive outcomes compared to the lines in which partners had mismatched gut microbiomes. Instead, we found that between‐partner concordance of maternally transmitted gut microbiota resulted in fewer offspring, and that this reduction was due to partial pre‐copulatory isolation as evidenced by reduced sperm transfer in theSelfXSelfline. This pattern is consistent either with microbiome‐mediated familiarity/kin recognition, or with absence of mate choice in crosses with mismatched microbiomes. We discuss our results in the light of recent research on the influence of extracellular microbial symbionts over insects' mating preferences.

     
    more » « less
  5. Synopsis

    The lower reproductive tract of female mammals has several competing functions including mating, tract health maintenance, and parturition. Diverse vaginal anatomy suggests interactions between natural and sexual selection, yet despite its importance, female copulatory morphology remains under-studied. We undertook a comparative study across the species-rich mammalian order Chiroptera (bats) with a focus on the suborder Yangochiroptera (Vespertilioniformes) to examine how female vaginal features may have coevolved with male penis morphology to minimize mechanical damage to their tissues during copulation. The penis morphology is diverse, presenting great potential for post-copulatory sexual selection and coevolution with the female morphology, but vaginas have not been carefully examined. Here we test the hypotheses that vaginal thickness and collagen density have coevolved with features of the male penis, including the presence of spines and a baculum. We present histological data from females of 24 species from 7 families of bats, and corresponding data on male penis anatomy. We also examine the role of phylogenetic history in the morphological patterns we observe. We found evidence that female vaginal thickness has coevolved with the presence of penile spines, but not with baculum presence or width. Collagen density did not appear to covary with male penile features. Our findings highlight the importance of considering interactions between the sexes in influencing functional reproductive structures and examine how these structures have been under selection in bats.

     
    more » « less