Behavior Outweighs Body Size in Mediating Male Reproductive Success in a Nest-Building Fish, Bluehead Chub

Behavioral Ecology and Sociobiology (2020) 74:148 https://doi.org/10.1007/s00265-020-02933-x ORIGINAL ARTICLE Behavior outweighs body size in mediating male reproductive success in a nest-building fish, bluehead chub Seoghyun Kim1,2 & Kasey C. Pregler1,2 & Elizabeth L. Cushman3 & Tanya L. Darden3 & Yoichiro Kanno1,2,4 Received: 10 June 2020 /Revised: 31 October 2020 /Accepted: 6 November 2020 # Springer-Verlag GmbH Germany, part of Springer Nature 2020 Abstract In polygamy, individuals interact in a non-random manner to shape reproductive networks. However, relative importance of behavior versus individual physical traits (e.g., body size) in determining access to partners and reproductive success varies by species and is poorly understood in small-bodied aquatic species for which direct observations are challenging in the wild. Here, we coupled automated individual tracking and genetic parentage techniques to characterize reproductive networks and their consequences on reproductive success in bluehead chub (Nocomis leptocephalus), a nest-building stream fish native to the southeastern USA. Fish were marked with 12-mm passive integrated transponder (PIT) tags, and loop-shaped PIT antennas were deployed around 18 nests to monitor behavioral encounters of 311 individuals (34 males and 277 females and immature males) during the spawning season in 2017. After spawning, genetic samples of 326 young-of-the-year fish (i.e., offspring) were collected. The mating system was polygynandrous, and factors affecting access to partners and reproductive success differed between males and females. Male body size did not affect number of encounters with females and reproductive success, instead behavior indexing reproductive effort (number and size of nests occupied) explained variation in reproductive success. On the contrary, body size was a key determinant of female reproductive success. Fecundity (i.e., number of eggs) increased with body size, and higher encounters rates with males did not result in higher reproductive success. In males and females, mating with more partners led to higher reproductive success, which may have contributed to the evolution and maintenance of polygynandry in this species. Significance statement Is bigger better? This question has been investigated with respect to animal mating behavior and reproductive success, and the answer appears to vary by species. Using an intensive individual-based approach with PIT antenna and molecular markers, we show that behavior outweighed body size in mediating reproductive success of males but not females of a nest-building stream fish. Males increased access to females and ultimately number of offspring by occupying larger and more nests, which are proxies of reproductive effort. In females, body size was more important than behavior in determining reproductive success, and behavior explained much less of variation in reproductive success. Diverse and complex reproductive patterns of males may explain why behavior outweighed body size in mediating reproductive success, a hypothesis that warrants further research across species with a gradient of mating systems and behavioral complexities. Keywords Reproductive interaction . Social network . Leuciscidae . Fitness . Individual tracking Seoghyun Kim and Yoichiro Kanno contributed equally to this work. Communicated by K. Lindström * Yoichiro Kanno 3 South Carolina Department of Natural Resources, Hollings Marine [email protected] Laboratory, 331 Fort Johnson Road, Charleston, SC 29412, USA 4 Graduate Degree Program in Ecology, Colorado State University, 1 Department of Fish, Wildlife, and Conservation Biology, Colorado Fort Collins, CO 80523-1474, USA State University, Fort Collins, CO 80523-1474, USA 2 Department of Forestry and Environmental Conservation, Clemson University, Clemson, SC 29634-0317, USA 148 Page 2 of 14 Behav Ecol Sociobiol (2020) 74:148 Introduction in oviparous species (Trippel et al. 1997; Soler et al. 1998; Nafus et al. 2015), and larger females produce larger and In polygamy, individuals mate with multiple partners, but higher-quality eggs (Barneche et al. 2018). The Bateman’s mating patterns are typically non-random (Andersson 1994; principle posits that female reproductive success does not typ- Reynolds 1996; McDonald and Pizzari 2016; Ziv et al. 2016). ically depend on number of mates, contrary to male reproduc- Some individuals mate with more partners than others, tive success (Jennions and Petrie 1997;Serbezovetal.2010; forming a complex web of reproductive interactions but see Jones et al. 2002). However, mate choice by females (Serbezov et al. 2010; McDonald and Pizzari 2016; Sabol affects reproductive success of their own and males via selec- et al. 2020). Characterizing reproductive interactions is critical tion of certain male characteristics such as body size, courtship to understanding behavioral ecology and evolution (Wey et al. display, coloration, and auditory signals (Andersson 1994; 2008; Leu et al. 2010), because the number of mates is a key McDonald and Potts 1994; Trainer and McDonald 1995; determinant of reproductive success, defined here as the num- Jennions and Petrie 1997). Mate choice by females is partic- ber of offspring assigned to individuals (Bateman 1948; ularly important in nest-building species in which males con- Emlen and Oring 1977; Andersson 1994; Jones et al. 2002). struct and defend their nests but females are mobile (Brooks However, much of our understanding of the relative impor- and Couldridge 1999;Leiseretal.2015). However, questions tance of behavior versus individual physical traits (e.g., body remain whether females choose mates based on characteristics size) in determining access to partners and ultimately repro- of males versus nests. Specifically, male body size is more ductive success comes from terrestrial taxa for which repro- important than nest characteristics in some studies (Oliveira ductive behavior may be readily observed in the wild or char- et al. 2000;Lehtonenetal.2007;Boseetal.2018) but not in acterization of reproductive networks can be facilitated due, others (Soler et al. 1998; Friedl and Klump 2000;Lehtonen for example, to prolonged parental care (e.g., birds and mam- and Lindström 2009). The mixed findings indicate that mate mals) (Friedl and Klump 2000; Wolff and Macdonald 2004; choice by female varies by species and environmental and Asher et al. 2008; Ziv et al. 2016; Sabol et al. 2020). social context (Emlen and Oring 1977; Wey et al. 2008; Males increase reproductive success by mating with more Lehtonen et al. 2010). partners in a variety of species (Bateman 1948; Reynolds Direct observations of reproductive behavior are diffi- 1996; Jones et al. 2002). Because sperm production is ener- cult for many species in the wild, but particularly for getically less costly than egg production (Ginsberg and Huck aquatic species that do not provide prolonged parental 1989;Wedelletal.2002), male reproductive success is limit- care for hatchlings. Molecular markers have facilitated ed by access to females (Bateman 1948; Jennions and Petrie characterization of animal mating systems, and they fre- 1997). Males compete with each other for access to females quently discover cryptic and complex reproductive net- (Emlen and Oring 1977; Andersson 1994), and outcomes of works among individuals (Marshall et al. 1998;Wolff this competition often depend on body size (Oliveira et al. and Macdonald 2004; Serbezov et al. 2010). More recent- 2000; Asher et al. 2008), which may also correlate with sec- ly, automated tracking systems (e.g., radio frequency ondary sexual characteristics such as body coloration in birds identification or RFID) have been added to the toolbox (McDonald and Potts 1994), antlers in mammals (Andersson of behavioral ecologists to quantify individual behavior 1994), and kypes (protruded hooks on the lower jaw) in fishes and interactions (Rehmeier et al. 2006; Newey et al. (Järvi 1990). In nest-building species, body size is important 2009; Sabol et al. 2018). Molecular markers and automat- because larger males construct nests of larger size or higher ed tracking complement each other and together provide quality (Soler et al. 1998; Lehtonen et al. 2007;Barber2013; richer information because animal tracking data reveal Bose et al. 2018) and outcompete smaller males for the most behavioral mechanisms that can explain variation in re- suitable nesting sites (Oliveira et al. 2000; Forstmeier 2002). productive success inferred from molecular techniques. However, smaller males may still reproduce by employing However, applications of both tools in combination have alternative reproductive behaviors, such as constructing more been limited in aquatic species. nests and segregating spawning temporally (Gross 1996; Bluehead chub (Nocomis leptochepalus)providesaunique Friedl and Klump 2000; Forstmeier 2002). Therefore, in ad- opportunity to study reproductive networks and their conse- dition to individual characteristics such as body size, male quences on reproductive success. They are a small-bodied reproductive success of nest-building species can be affected minnow (Leuciscidae), and adult body size ranges between by behavioral variation among individuals (Lehtonen and 70 and 200 mm (Lanchner 1952; Jenkins and Burkhead Lindström 2009;Barber2013). 1994). Breeding males develop the blue head with tubercles, In females, body size and behavior similarly determine and males are larger than females at maturity (Jenkins and their reproductive

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