Elsevier

Zoology

Volume 142, October 2020, 125816
Zoology

Reproduction in the pitviper Bothrops jararacussu: large females increase their reproductive output while small males increase their potential to mate

https://doi.org/10.1016/j.zool.2020.125816Get rights and content

Highlights

  • This species shows one of the highest sexual size dimorphisms in snakes.

  • The evolution of such extreme dimorphism was likely driven fecundity selection.

  • A large body size allows females to increase their reproductive output.

  • Males show a potentially longer ability to mate.

  • Bothrops have undergone multiple evolutionary shifts in the timing of spermiogenesis.

Abstract

Reproductive traits vary widely within and among snake species, and are influenced by a range of factors. However, additional studies are needed on several species, especially on tropical snake faunas, to fully understand the patterns of reproductive variation in snakes. Here, we characterized the reproductive biology of B. jararacussu from southeastern and southern Brazil. We combined macroscopic and microscopic examinations of the reproductive system of museum specimens with observations of free-ranging snakes to characterize size at sexual maturity, sexual size dimorphism (SSD), reproductive output, and male and female reproductive cycles. We compared our data with published literature and discuss the factors that may play a role in shaping the reproductive patterns in the species and the genus. Bothrops jararacussu shares several characteristics with its congeners such as autumn mating season, obligatory sperm storage in the female reproductive tract, seasonal timing of parturition (summer-autumn), female-biased SSD, maturity at larger body sizes in females, and a positive relationship between body size and litter size. These characteristics seem phylogenetically conserved in Bothrops. On the other hand, B. jararacussu exhibits some unique characteristics such as a high degree of SSD (one of the highest values recorded in snakes), a large female body size, and a large litter and offspring size, which are among the largest recorded in the genus. Moreover, larger females reproduce more frequently than smaller conspecifics. These characteristics may be collectively interpreted as the result of a strong selection for increased fecundity. Other peculiarities of the species include an asynchrony between spermiogenesis (summer-autumn) and the peak of SSK hypertrophy (autumn to spring) and a prolonged production of SSK granules. Because SSK hypertrophy and mating are androgen-dependent in snakes, the prolonged SSK hypertrophy suggests that male B. jararacussu may prolong their potential to mate (compared with its congeners), which may increase their reproductive success. Our results and previous literature collectively suggest that, in Bothrops, the evolution of SSD is driven by fecundity selection, variation in reproductive output is influenced by variation in female body size, and the timing of spermiogenesis is influenced by other factors in addition to temperature. We also suggest that male Bothrops have undergone multiple evolutionary shifts in the timing of spermiogenesis.

Introduction

Reproductive traits vary widely within and among species of squamate reptiles. Variation in reproductive traits is often attributed to the occupation of regions with different environmental factors (Mesquita and Colli, 2003; Ji and Wang, 2005). For instance, temperate-zone squamates usually reproduce seasonally, with females ovipositing/giving birth during the warmer months, whereas tropical squamates tend to exhibit more variable cycles, with females reproducing over longer periods (James and Shine, 1985; Seigel and Ford, 1987). In turn, similarity in reproductive traits often occurs even in populations or closely related species inhabiting environmentally distinct areas. For instance, low and invariant clutch sizes characterize entire lineages of lizards from drastically different environments (Shine and Greer, 1991). Such similarity in reproductive patterns is often attributed to phylogenetic conservatism, since closely related species tend to exhibit similar traits because of their common ancestry (Harvey and Pagel, 1991). Additionally, variation in several reproductive traits is also attributed to variation in body size and its correlates, such as abdominal volume. Body size influences reproductive output, i.e., clutch/litter size, offspring size, and reproductive frequency. In species with variable clutch/litter size, larger females tend to produce more and/or larger offspring (Dunham et al., 1988; Shine, 1994). Moreover, in many species, larger females tend to reproduce more often than smaller conspecifics (Seigel and Ford, 1987). These patterns are evident across species and are also influenced by the environment and phylogeny (Dunham et al., 1988; Shine, 1994; Bellini et al., 2017).

In snakes, previous studies have shown that female reproductive phenology tends to be phylogenetically conserved (Shine, 1989; Pizzatto et al., 2008a, 2008b; Marques et al., 2013b; Shine et al., 2014). However, given the remarkable diversity in snake reproductive strategies (Seigel and Ford, 1987; Shine, 2003), a complex array of conservative and variable reproductive traits is also evident. For instance, the timing of vitellogenesis varies geographically within some species (e.g., Pizzatto et al., 2008b) but not in others (see examples in Aldridge et al., 2009). In addition, the possibility that phylogeny also constrains male reproductive patterns needs confirmation, as many studies on male reproduction lack direct evidence supporting the timing of spermatogenesis (reviewed in Mathies, 2011). Although clutch/litter size increases with maternal body size in most species, this relationship is not evident in all species (Seigel and Ford, 1987). Similarly, reproductive frequency increases with increasing female body size in several species (Blem, 1982; Seigel and Ford, 1987), but in others, it decreases with body size (Shine et al., 1998) or is maximized at intermediate body sizes (Madsen and Shine, 1996; Bonnet et al., 2000). Thus, it remains difficult to generalize the patterns of reproductive variation in snakes and, consequently, we need additional studies on several snake species, especially on tropical snake faunas.

Lancehead snakes (genus Bothrops) are an excellent study system in which to investigate factors that influence reproduction. The genus contains 45 species widely distributed over a range of climatically distinct ecoregions in Central and South America (Carrasco et al., 2019; Uetz et al., 2019). Moreover, Bothrops species vary greatly in body sizes, body shapes, and macrohabitat use (Martins et al., 2001), and their phylogenetic relationships are reasonably known (Alencar et al., 2016), thus facilitating the interpretation of the evolution of reproductive patterns. Female reproductive biology has been investigated in a reasonable number of Bothrops (Solórzano and Cerdas, 1989; Sazima, 1992; Almeida-Santos and Orsi, 2002; Almeida-Santos and Salomão, 2002; Valdujo et al., 2002; Nogueira et al., 2003; Hartmann et al., 2004; Monteiro et al., 2006; Nunes et al., 2010; Marques et al., 2013a; Barros et al., 2014a, 2014b; Leão et al., 2014; Almeida-Santos et al., 2017; Silva et al., 2019b). Irrespective of the diversity of habitats in which they occur (ranging from seasonal to aseasonal environments), female Bothrops reproduce seasonally and share similarities in various reproductive characteristics likely inherited from their ancestor (Almeida-Santos and Salomão, 2002). For instance, in most Bothrops species studied, mating occurs primarily in autumn, with females at early vitellogenesis. Consequently, females must store sperm in their reproductive tract until ovulation in spring, and parturition occurs mostly in summer but may extend to autumn (Almeida-Santos and Salomão, 2002; for an exception, see Silva et al., 2019b). Moreover, in all Bothrops species studied so far, females typically grow larger and mature at larger body sizes than males (e.g., Solórzano and Cerdas, 1989; Valdujo et al., 2002; Nogueira et al., 2003; Silva et al., 2019b). In contrast, litter size seems highly variable interspecifically (Almeida-Santos and Salomão, 2002) but typically increases with maternal body size intraspecifically (e.g., Solórzano and Cerdas, 1989; Nogueira et al., 2003; Hartmann et al., 2004). Male reproductive patterns have been less studied, but Almeida-Santos and Salomão (2002) hypothesized that spermatogenesis is also seasonal (occurring in spring-summer) and phylogenetically conserved. Recent studies have generally corroborated this hypothesis (Barros et al., 2014b; Almeida-Santos et al., 2017; Silva et al., 2019b; but see Barros et al., 2014a). However, male reproductive cycles have been investigated histologically in few Bothrops and therefore this hypothesis has not yet been tested.

This study describes the reproductive biology of B. jararacussu, a species found in southeastern South America (Campbell and Lamar, 2004; Marques et al., 2004). In Brazil, B. jararacussu inhabits primarily lowland (from 0-700 m of elevation) Atlantic forest areas along southeastern and southern regions (Nogueira et al., 2019). This species is a dietary generalist, and individuals are found active on the ground by day and night (Martins et al., 2002; Marques and Sazima, 2004). Female B. jararacussu have rather stout bodies and attain one of the largest sizes in the genus (Martins et al., 2001). However, no study has addressed its reproductive biology. We combined macroscopic and microscopic examinations of the reproductive system of museum specimens with observations of free-ranging and recently captured snakes to characterize size at sexual maturity, sexual size dimorphism, reproductive output, and male and female reproductive cycles. We address the following questions: (1) Is there sexual size dimorphism, and if so, what is the magnitude and the potential causes of such dimorphism? (2) Does the large female size result in an increase in reproductive output, compared with congeners? (3) Does the male reproductive phenology resemble that of its congeners, reflecting a conserved pattern? We also discuss the factors that may play a role in shaping the reproductive patterns observed in the genus.

Section snippets

Specimens and area

We collected reproductive data from 609 specimens housed in Brazilian museums (Supplementary Table S1). Specimens were collected between 1914-2016 in the Atlantic forest areas of the states of Rio de Janeiro, São Paulo, Paraná, and Santa Catarina (between 21 and 27 °S, 4–1000 m above sea level; Supplementary Table S1). The climate in this portion of the Atlantic Forest is seasonal. Warmer temperatures occur from spring (October-December) to summer (January-March) and are associated with higher

Body sizes, sexual maturity, and sexual size dimorphism

The smallest adult male measured 460 mm SVL, and all males larger than 610 mm SVL were adults. Most individual males (28 of 39; 76%) between 460-610 mm SVL were adults. The smallest adult female was pregnant and measured 800 mm SVL, and all females larger than 1010 mm SVL were adults. Most individual females (26 of 36, 72%) between 800-1010 mm SVL were adults. Therefore, males attained sexual maturity at smaller body sizes than females. Adult females averaged 1150.6 ± 144.7 mm SVL (range =

Sexual maturity, sexual size dimorphism, and reproductive output

As expected, female B. jararacussu mature at larger body sizes than males, and litter size increases with maternal body size. These patterns are common in snakes (Seigel and Ford, 1987; Shine, 1994), including Bothrops (Solórzano and Cerdas, 1989; Sazima, 1992; Valdujo et al., 2002; Hartmann et al., 2004; Monteiro et al., 2006; Marques et al., 2013a; Barros et al., 2014a, 2014b; Leão et al., 2014; Almeida-Santos et al., 2017; Silva et al., 2019b). Therefore, maturity at larger body sizes allows

Conclusions

Bothrops jararacussu shares several characteristics with its congeners such as autumn mating season, obligatory sperm storage in the female reproductive tract, timing of parturition, female-biased SSD, maturity at larger body sizes in females, and increases in litter size with increasing body size. We suggest that these characteristics are phylogenetically conserved in Bothrops. On the other hand, this pitviper has evolved some unique characteristics such as a high degree of SSD (one of the

Declaration of Competing Interest

The authors declare no conflict of interest.

Acknowledgements

We thank Giuseppe Puorto, Francisco Franco, Paulo Passos, and Júlio Moura-Leite for allowing us to examine specimens under their care. We also thank Nina Furnari for assistance in data collection, Valdir Germano for assistance in the laboratory, Luciana Sato for assistance with the histochemical tests, Marta Antoniazzi and Carlos Jared for kindly allowing access to microscopic equipment, Fernanda Stender-Oliveira and Rodrigo Scartozzoni for providing unpublished information on mating and

References (113)

  • R.D. Aldridge et al.

    Evolution of the mating season in the pitvipers of North America

    Herpetol. Monogr.

    (2002)
  • R.D. Aldridge et al.

    The reproductive cycle and estrus in the colubrid snakes of temperate North America

    Contemp. Herpetol.

    (2009)
  • R.D. Aldridge et al.

    Reproductive biology of the massasauga (Sistrurus catenatus) from South-Central Illinois

  • R.D. Aldridge et al.

    The sexual segment of the kidney

  • R.D. Aldridge et al.

    Seasonal timing of spermatogenesis and mating in squamates: A reinterpretation

    Copeia

    (2020)
  • S.M. Almeida-Santos

    Modelos reprodutivos em serpentes: estocagem de esperma e placentação em Crotalus durissus e Bothrops jararaca (Serpentes: Viperidae)

    (2005)
  • S.M. Almeida-Santos et al.

    Reproductive biology of the Brazilian lancehead, Bothrops moojeni (Serpentes, Viperidae), from the state of São Paulo, southeastern Brazil

    South Am. J. Herpetol.

    (2017)
  • S.M. Almeida-Santos et al.

    Biologia reprodutiva de serpentes: recomendações para a coleta e análise de dados

    Herpetol. Bras.

    (2014)
  • S.M. Almeida-Santos et al.

    Ciclo reprodutivo de Crotalus durissus e Bothrops jararaca (Serpentes, Viperidae): morfologia e função do oviduto

    Rev. Bras. Reprodução Anim.

    (2002)
  • S.M. Almeida-Santos et al.

    Reproduction in Neotropical pitvipers, with emphasis on species of the genus Bothrops

  • V.A. Barros et al.

    Is rainfall seasonality important for reproductive strategies in viviparous Neotropical pitvipers? A case study with Bothrops leucurus from the Brazilian Atlantic Forest

    Herpetol. J.

    (2014)
  • V.A. Barros et al.

    Reproductive biology of Bothrops erythromelas from the Brazilian Caatinga

    Adv. Zool.

    (2014)
  • V.A. Barros et al.

    Male reproductive cycle of Bothrops pubescens(Serpentes, Viperidae) from Southern Brazil

    South Am. J. Herpetol.

    (2020)
  • V.A. Barros et al.

    Reproductive biology of the neotropical rattlesnake Crotalus durissus from northeastern Brazil: a test of phylogenetic conservatism of reproductive patterns

    Herpetol. J.

    (2012)
  • E.A. Bassi et al.

    Reproductive cycle and sperm storage of female coral snakes, Micrurus corallinus and Micrurus frontalis

    Amphibia-Reptilia

    (2019)
  • S.J. Beaupre

    Annual variation in time-energy allocation by timber rattlesnakes (Crotalus horridus) in relation to food acquisition

  • G.P. Bellini et al.

    Is xenodontine snake reproduction shaped by ancestry, more than by ecology?

    Ecol. Evol.

    (2017)
  • C.R. Blem

    Biennial reproduction in snakes: an alternative hypothesis

    Copeia

    (1982)
  • X. Bonnet et al.

    Reproductive versus ecological advantages to larger body size in female snakes, Vipera aspis

    Oikos

    (2000)
  • H.B. Braz et al.

    Uterine and eggshell modifications associated with the evolution of viviparity in South American water snakes (Helicops spp.)

    J. Exp. Zool. Part B Mol. Dev. Evol.

    (2018)
  • H.B. Braz et al.

    Reproductive ecology and diet of the fossorial snake Phalotris lativittatus in the Brazilian Cerrado

    Herpetol. J.

    (2014)
  • H.B. Braz et al.

    Reproductive biology of the fossorial snake Apostolepis gaboi (Elapomorphini): a threatened and poorly known species from the Caatinga region

    South Am. J. Herpetol.

    (2019)
  • J.A. Campbell et al.
    (2004)
  • P.A. Carrasco et al.

    A new species of Bothrops (Serpentes: Viperidae: Crotalinae) from Pampas del Heath, southeastern Peru, with comments on the systematics of the Bothrops neuwiedi species group

    Zootaxa

    (2019)
  • R.M. Cox et al.

    The evolution of sexual size dimorphism in reptiles

  • A.E. Dunham et al.

    Life history patterns in squamate reptiles

  • N.B. Ford et al.

    The influence of female body size and shape on the trade-off between offspring number and offspring size in two viviparous snakes

    J. Zool.

    (2015)
  • S.R. Goldberg

    Reproduction in the tiger rattlesnake, Crotalus tigris (Serpentes: Viperidae)

    Texas J. Sci.

    (1999)
  • S.R. Goldberg

    Reproduction in the blacktail rattlesnake, Crotalus molossus (Serpentes: Viperidae)

    Texas J. Sci.

    (1999)
  • S.R. Goldberg

    Reproduction in the speckled rattlesnake, Crotalus mitchellii (Serpentes: Viperidae)

    Bull. South. Calif. Acad. Sci.

    (2000)
  • S.R. Goldberg

    Reproduction in the twin-spotted rattlesnake, Crotalus pricei (Serpentes: Viperidae)

    West. North Am. Nat.

    (2000)
  • S.R. Goldberg et al.

    Reproduction in the Baja California rattlesnake, Crotalus enyo (Serpentes: Viperidae)

    Bull. South. Calif. Acad. Sci.

    (2003)
  • S.R. Goldberg et al.

    Seasonal testicular histology of the colubrid snakes, Masticophis taeniatus and Pituophis melanoleucus

    Herpetologica

    (1975)
  • S.R. Goldberg et al.

    Reproduction in the Mojave rattlesnake, Crotalus scutulatus (Serpentes: Viperidae)

    Texas J. Sci.

    (2000)
  • P.T. Gregory et al.

    Snake litter size = live young + dead young + yolks

    Herpetol. J.

    (1992)
  • M.T. Hartmann et al.

    Reproductive biology of the southern Brazilian pitviper Bothrops neuwiedi pubescens (Serpentes, Viperidae)

    Amphibia-Reptilia

    (2004)
  • P.H. Harvey et al.

    The Comparative Method in Evolutionary Biology

    (1991)
  • C.R. Hendry et al.

    Ecological divergence and sexual selection drive sexual size dimorphism in new world pitvipers (Serpentes: Viperidae)

    J. Evol. Biol.

    (2014)
  • A.T. Holycross et al.

    Reproduction in northern populations of the ridgenose rattlesnake, Crotalus willardi (Serpentes: Viperidae)

    Copeia

    (2001)
  • J.B. Iverson et al.

    Understanding reproductive allometry in turtles: A slippery “slope”

    Ecol. Evol.

    (2019)
  • Cited by (15)

    • Clinical implications of ontogenetic differences in the coagulotoxic activity of Bothrops jararacussu venoms

      2021, Toxicology Letters
      Citation Excerpt :

      Belonging to the Bothrops genus, which is responsible for the majority of snakebite accidents in Brazil (Chippaux, 2015), B. jararacussu is included as a Category 1 by WHO as a species that has medical relevance, due to the number of accidents and morbidity of the snake envenomation (WHO, 1999). B othrops jararacussu is characterized by its sexual dimorphism, in which females are larger than males, thus being able to produce a high volume of venom (Melgarejo, 2009; Milani et al., 1997; Silva et al., 2020). This species is distributed in tropical forests in Brazil, southern Bolivia, Paraguay, and Northeastern Argentina (Melgarejo, 2009; Milani et al., 1997).

    View all citing articles on Scopus
    View full text