Mating decisions can be affected by intrasexual competition and sensitive to operational sex-ratio (OSR) changes in the population. Conceptually, it is assumed that both male and female mate- competition may interfere with female reproductive decisions. Experimentally, however, the focus has been on the effect of male competition on mate choice. In many species with paternal care as in the common goby Pomatoschistus microps, the OSR is often female-biased and female mate- competition for access to available nesting males occurs. Using the same protocol for 3 experi- ments testing the effect of a perceived risk of female mate-competition, I studied female preferen- ces for nest-holding males differing in its nest size (large/small), body size (large/small), and nest status (with/without eggs already in nest) and measured mating decisions, spawning latencies, and clutch size. Regardless of the social context, females preferred males with larger nests. A prefer- ence for large males was only expressed in presence of additional females. For nest status, there was a tendency for females to prefer mating with males with an empty nest. Here, female–female competition increased the propensity to mate. The results of this study show that females are sen- sitive to a female competitive social environment and suggest that in choice situations, females respond to the social context mainly by mating decisions per se rather than by adjusting the clutch size or spawning latency. Females base their mating decisions not only on a male’s nest size but also on male size as an additional cue of mate quality in the presence of additional females. Key words: audience effect, intrasexual competition, mate sampling, parental care, Pomatoschistus microps, sex-roles, size. Studies of sexual selection have traditionally been focusing on Specifically, the interaction between female–female competition and female choice or male–male competition (Andersson 1994; Clutton- its effects on female mating preferences and sexual selection has Brock and Huchard 2013), or far less frequently their interaction received very little attention, even though its importance has been (Kangas and Lindstro ¨ m 2001; Lehtonen and Lindstro ¨ m 2009, acknowledged (Jennions and Petrie 1997; Cotton et al. 2006; Rosvall reviewed in Wong and Candolin 2005). Berglund et al. (2005) 2011; Rubenstein 2012; Kvarnemo and Simmons 2013). emphasize that instead of splitting into the dichotomy of mate choice In particular, species with male parental care (Owens et al. and intrasexual competition, there is rather a combination of both. 1994; Almada et al. 1995; Kvarnemo et al. 1995; Borg et al. 2002; However, most recent studies are still concentrating on either one or Forsgren et al. 2004), or significant male nutritional investment in the other, not at potential interactions of both. The opposite phenom- the eggs (Gwynne and Simmons 1990; Simmons and Kvarnemo ena, male choice and female–female competition, have been less 2006) often show female–female competition for access to male frequently studied (Andersson 1994; Rosvall 2011; Clutton-Brock and parental investment. In such cases, parental investment defined as Huchard 2013; Kvarnemo and Simmons 2013; Clutton-Brock 2017). “any investment by the parent in an individual offspring that V C The Author(s) (2018). Published by Oxford University Press. 351 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact firstname.lastname@example.org Downloaded from https://academic.oup.com/cz/article-abstract/64/3/351/4961447 by Ed 'DeepDyve' Gillespie user on 21 June 2018 352 Current Zoology, 2018, Vol. 64, No. 3 increases the offspring’s survival and reproductive success at the cost challenging environment or social context (forced mating versus free of the parent’s ability to invest in other current or future offspring” mate choice: Lindstro ¨ m and Kangas 1996; supply of oxygen: (Smiseth et al. 2012) may differ little between the 2 sexes. Reynolds and Jones 1999; filial cannibalism and female body size: Consequently, sex-roles, defined by which sex has the higher paren- Andre ´ n and Kvarnemo 2014; reviewed: Qvarnstro ¨ m 2001; Wong tal investment and is thus limiting the reproduction of the other sex and Candolin 2005). (Trivers 1972; Kokko and Jennions 2008), can rapidly change in It is widely acknowledged that mating decisions are affected by response to the availability of the opposite sex in the mating pool, intrasexual competition for access to gametes or resources required for mating (Andersson 1994; Wong and Candolin 2005; Ahnesjo ¨ expressed as the operational sex-ratio (OSR) (Emlen and Oring et al. 2008; Candolin and Wong 2008; Brooks and Griffith 2010)or 1977; Kvarnemo and Ahnesjo ¨ 1996; Borg et al. 2002; Forsgren et al. presence of an audience (Plath et al. 2008; Ziege et al. 2009). 2004; Simmons and Kvarnemo 2006). Thus, female–female compe- Therefore, underlying preferences may be constrained by intrasexual tition should occur when access to males or breeding resources such interactions, which may range from simple detection probability or as nest sites limits reproduction. reduced mate assessment opportunities to contest competition and In gobies, males exclusively provide parental care in their nests to which females add their eggs. Those nests are maintained and hence involvement in aggressive interactions, overridden choices, or defended by territorial males. Males may simultaneously accommo- switch to alternative mating tactics, leading to variation in the date clutches of several females in their nests (Miller 1984). While extent and direction of sexual selection. However, it is usually tested most species with paternal care are assumed to follow the general with a focus on males, for example, male–male competition compro- scheme of choosy females, male courtship displays and male–male mising the ability of females to evaluate mates (Kangas and competition (Andersson 1994), some gobies stick out from that Lindstro ¨ m 2001; Lehtonen and Lindstro ¨ m 2009; reviewed in Wong well-known picture: female courtship behavior occurs and males and Candolin 2005). The current experiments will contribute to may be choosy (Magnhagen 1998; Borg et al. 2002; Forsgren et al. understanding the effect of female competition on female preferen- 2004), the OSR fluctuates and is often female-biased (Borg et al. ces. This is especially relevant as in nature for many fish species with 2002, 2006; Forsgren et al. 2004; Mu ¨ ck and Heubel 2018), and male parental care, a female-biased OSR is common, and hence females often compete for access to nesting males (Borg et al. 2002; strength and direction of sexual selection may shift (Wacker et al. Forsgren et al. 2004; Mu ¨ ck and Heubel 2018). 2013, 2014). Furthermore, in some gobiid species, also females are The aim of this study is to test the effect of a perceived risk of colorful (Takahashi 2000; Amundsen and Forsgren 2001; Massironi female–female competition on female mate choice decisions. Thus, I et al. 2005; Svensson et al. 2009). Especially in the small and short- will conduct female mate choice trials with binary choices for stimuli lived common goby Pomatoschistus microps, both males and of varying quality: (1) male size (large versus small), (2) males with females mate repeatedly during a single reproductive season (Miller different nest sizes (large versus small), and (3) males with different 1975). However, males can only accommodate a relatively small nest status (already with versus without eggs) in female-competitive number of egg clutches in their nests (Magnhagen and Vestergaard compared with non-competitive situations, imposed by the presence 1993; Pampoulie et al. 2001; Mu ¨ ck and Heubel 2018). Hence, in or absence of audience females. As female mating decisions may be this system, I expect female–female competition to play an impor- expressed in various ways, I measured the propensity of mating, the tant role despite non-reversed sex-roles, that is, higher potential mating decision, the latency until spawning, and the clutch size. reproductive rates (PRR) in males than in females and higher costs Under competitive situations, females can respond by being less of reproduction in females and hence still females limiting reproduc- choosy and more likely to make compromised, suboptimal but tion in this species (Clutton-Brock and Vincent 1991; Ahnesjo ¨ et al. faster decisions with regard to mate and nest attributes and hence 2008). Results from an earlier study on reproduction under different compromising quality for lower costs of mate choice given a OSRs and competitive environments in common gobies show that perceived threat of limited future mating opportunities. Given this females suffer from intrasexual competition and adjust their repro- scenario, I would expect females to show no preferences, shorter ductive decisions to compensate for reduced future chances of repro- spawning latencies, and unadjusted clutch sizes. Alternatively, ductive success (Heubel et al. 2008). Female–female competition females may exhibit preferences for specific or additional cues, can be expected to affect not only reproductive effort, but also adopt choosy mate sampling strategies, and hence rather adjust female mate choice behavior (Heubel et al. 2008; Hayes et al. 2016). mating decisions to increase the benefits of their current mating For gobies, studied in standard mate choice trials with a choos- decision by carefully basing their mate choice on further cues ing focal female and 2 simultaneous male stimuli, there is a general relevant under the current circumstances. The latter would rather preference for larger, heavier, and better-conditioned males (Borg lead to lower mating propensities, stronger preferences, longer et al. 2006; Lehtonen et al. 2007; Kalb et al. 2016) and males with spawning latencies, and adjusted clutch sizes. Thus, female elevated levels of fanning, paternal care, and courtship activity competition may either commence, reinforce, or weaken female (Lindstro ¨ m et al. 2006; Amorim et al. 2013). However, opposite or preferences for males with larger nests, larger body size, and nests fluctuating patterns of mating preferences may exist (Svensson and that already contain eggs. Forsgren 2003; Borg et al. 2006; Lehtonen et al. 2010; Lehtonen 2012; Locatello et al. 2016). Females also prefer larger and more elaborate nests (Lindstro ¨ m 1992; Jones and Reynolds 1999; Materials and Methods Lehtonen et al. 2007; Kalb et al. 2016). In addition, previous studies found that in many species with male parental care, females prefer Experimental paradigm to lay eggs in nests that already contain eggs (Kraak and Groothuis In binary choice tests with or without additional audience females in 1994; Jamieson 1995; Forsgren et al. 1996a; Requena and Machado an adjacent compartment, I tested the effect of female–female 2015). However, it is still not well understood why such preferences competition on female mate choice preferences for nest size (large exist and how they change in a competitive environment (Lehtonen versus small), male size (large versus small), and nest status (with or and Lindstro ¨ m 2009; Lindstro ¨ m and Lehtonen 2013) or otherwise without eggs) in an annual benthic fish with paternal care. Downloaded from https://academic.oup.com/cz/article-abstract/64/3/351/4961447 by Ed 'DeepDyve' Gillespie user on 21 June 2018 Heubel Female competition alters mating preferences 353 Study species females attached their eggs in a single layer when spawning The common goby is a small short-lived marine fish with male (Lindstro ¨ m 2001; Vallon et al. 2016). After measuring and tagging, males were transferred to their parental care. On shallow soft bottoms, males build and defend nests under mussel shells or other hard structures by excavating a individual sections in experimental tanks. Experimental tanks were (without additional rear compartment) 70 cm 25 cm or (equipped cavity in the sand and gathering sand on top of the shell (Nyman with a parallel divider to offer an additional rear 15 cm wide com- 1953). Eggs are deposited on the ceiling in a single layer of these partment for audience females along the long side of the tank) 60 – burrows and receive paternal care until hatching through fanning 70 40 cm (Figure 1A). and protection from predators (Vestergaard 1976). Natural nest availability, nest substrates, and nest characteristics vary greatly Study design across the Baltic Sea (Nyman 1953; Magnhagen and Vestergaard Using the same general experimental framework of always having 1991; Forsgren et al. 1996b; Mu ¨ ck and Heubel 2018). Males can half of the experimental tanks either with or without 6 additional receive several egg clutches of different females, depending on the females in the adjacent compartment as a perceived risk of female size of the nest, and care for all eggs simultaneously during a single competition at a naturally realistic level for the tested population breeding cycle (Magnhagen and Vestergaard 1993). Competition for (personal observation), I tested female mating preferences for males mussel shells and other nest structures can be fierce (Borg et al. differing in nest size (experiment 1), male size (experiment 2), and 2002; Mu ¨ ck and Heubel 2018) and large males often manage to nest status (experiment 3) (Figure 1B). To control for potential side obtain larger shells, which can also result in more eggs in their nest biases, I alternated the assignment of the 2 alternative stimulus types (Magnhagen and Vestergaard 1993). The OSR and the extent of between the left and the right end of the tank across both treatments female–female competition varies spatially and temporally (Borg in all 3 experiments. As response variables, I measured female mat- et al. 2002; Mu ¨ ck and Heubel 2018), rendering the common goby a ing propensity, mating decision, the latency until spawning, and the good model to study the effect of perceived risk of female–female clutch size. competition on female mating preferences for direct and extended male phenotypes. Experimental procedure Both males had time to build nests overnight in the assigned male Fish collection and housing compartment at either end of the tank, which refrains males from All behavioral experiments were conducted during the major part of interacting with each other during the phase of setting up territories the common goby breeding season in June and July in the northern and nest building (Lehtonen et al. 2007; Lehtonen and Lindstro ¨m Baltic Sea at Tva ¨ rminne Zoological Station, Finland. Fish were col- 2009). If one or both males did not build nests within 24 h, it was lected from the field in the Tva ¨ rminne Archipelago by hand trawling replaced by a similarly sized male. Once both males had erected in Sandvik, a bay at Henriksberg (latitude 59.83 N, longitude their territories, I introduced the 6 additional females into the rear 23.14 E) near the station. For at least 3 and up to 10 days post- compartment in tanks assigned to the female competition treatment catching fish were maintained in large (size 70 cm 50 cm or and let them acclimatize for 24 h with visual contact to the 2 males. 80 cm 80 cm), sex-separated stock tanks. Each tank had a 2–4 cm The 6 audience females were chosen randomly from a stock tank. sand layer and a continuous flow-through of brackish sea water. To insure that the audience was perceived by the test female as com- Water quality, light conditions, and temperature followed natural petitors imposing a threat for female mate-competition and chal- conditions. Non-transparent sides of tank prevented interaction lenging the access to mates rather than just as bystanders, the group between tanks. Fish were fed once a day ad libitum with frozen chi- of female competitors always contained at least 1 female that was ronomid larvae with supplementary feeding with live mysids larger than the focal female and at least 2 females ready to spawn as Neomysis integer, and uneaten food was removed. After the experi- indicated by roundness. ment, fish were released back into their natural habitat. Then a single ready-to-spawn female was introduced into the central section for overnight acclimation. The female was able to General procedures visually inspect both males and—in the female competition treat- Before the experiment, I measured total body length (to the nearest ment—the audience females in the rear compartment. 1 mm) and wet body weight (to the nearest 0.001 g) in all individu- The mating trial started by lifting the clear dividers that pre- als. To be able to track male nest ownership and identity, all males vented the focal female from accessing the 2 males. Trials were only were individually marked with 2 color marks (injected subcutane- started when both males and the focal female and at least 3 of the ously on the dorsal surface of the body to the left and the right of audience females were visible and active. the dorsal fin) using visible implant elastomer tags (Northwest The female and the 2 males were allowed to interact freely. Marine Technology, USA). However, territorial males stayed usually closely attached to their Experimental tanks were divided into 3 partitions with 2 clear nests at the 2 opposite ends of the tank interacting with the females removable, tightly fitted dividers with small holes for water flow but only rarely with the other male. I regularly checked nest owner- between sections. Some of the tanks also had a clear permanent ship and status (Kalb et al. 2016). If no mating occurred within 6 h, divider with small holes to provide an additional long rear compart- I checked again late in the evening and re-checked in the morning. ment to hold the additional audience females providing a perception Replicates without spawning occurred by the next morning were of a female-competitive environment (Figure 1A). To prevent male– considered as a decision not to mate and replicates with inactive, male interactions, the 2 opposing outer sections were used for the 2 buried males or focal females were dismissed. After 24 h, I termi- stimulus males, both equipped with a halved flowerpot as a nesting nated the trial and recorded the nest ownership and nest status, and resource (Lehtonen and Lindstro ¨ m 2009). Each pot had a removable the presence of eggs in their nests. Clutches were removed and pho- piece of a transparent plastic sheet fit on the inside onto which tographed for egg counts. Downloaded from https://academic.oup.com/cz/article-abstract/64/3/351/4961447 by Ed 'DeepDyve' Gillespie user on 21 June 2018 354 Current Zoology, 2018, Vol. 64, No. 3 Figure 1. (A) The setup of experimental tanks. Depicted is the design including additional audience females in the adjacent compartment. For all experimental runs, half of the tanks were with or without female competitors, respectively. Removable dividers are drawn as dashed lines. After an acclimation period, the female had free access to both nests and males. (B) The design of the experiment. Females chose between nests (1) and males (2) that were either small or large (indicated by differently sized symbols, respectively). In Experiment 3, females chose between males with nests that either had eggs or where eggs had been removed. Experiments Data handling and statistical analysis In the nest-size experiment (1), the female had to choose between Females always had the option not to spawn at all within the experi- males with large (halved flowerpots 4.5 cm ø, 4 cm depth) and mental time frame given the set of offered potential mates. small nests (3.5 cm ø, 3 cm depth). The large artificial nest repre- Therefore, I tested the propensity to mate, specifically, whether the sents the size of large natural nests in the local population (Mu¨ck probabilities for spawning to take place differed between the social and Heubel 2018) and fits 2–3 clutches (personal observation). contexts. For all other analyses on mating decisions given the 2 The small artificial nest represents the average size of nests in the offered alternative stimuli, trials with spawnings in both nests (3 local population and fits about 1–2 clutches (Mu¨ck and Heubel cases) and trials without any spawning were excluded. For cases 2018). Males were size matched (n ¼ 80, size difference with clear signs of filial cannibalism, that is, residues of mucus but 0.56 0.05 mm, mean6 SE). no eggs in places on the spawning substrate (Mu ¨ ck and Heubel In the male-size experiment (2), I tested female mating preferen- 2018), I excluded data for clutch size. In the nest-size experiment ces for a large versus a small male while nests were size-matched (1), there was an initial n of 126 trials leading to a final sample size (halved flowerpots 4.5 cm ø, 4 cm depth). The size difference of n ¼ 68 for trials in which mating took place in 1 nest (n ¼ 67 for between the 2 males was at least 3 mm (n ¼ 100, 5.16 0.15 mm) clutch size). In the male-size experiment (2), I analyzed n ¼ 53 trials (mean6 SE). This size difference is equivalent to the standard devia- with data for spawning, n ¼ 50 for latency, and n ¼ 48 for clutch tion of the mean male size for males with observed mating success in size (out of 102 trials in total). In the nest-status experiment (3) out the studied population (unpublished data). of initially n ¼ 38 trials, 31 with matings were used in the analysis. In the nest-status experiment (3), I offered the choice between To control for any side biases, the assignment of the 2 different stim- males with nests that already contain eggs versus without eggs. uli to either the left or right side of the aquaria was continuously Males and nests (4.5 cm ø) were size-matched. The males started alternated in both social contexts and all 3 experiments. To refute with identical initial conditions in terms of mating status: both occurrence of side-biases, I tested whether the probability for males had already mated with another female the previous day. I spawning differed on the left and the right side. There was no differ- removed the initial female egg donors and randomly replaced 1 ence between experiments and over all experiments spawning took males’ clutch by a clean piece of transparent plastic. place with the stimulus male on the left 72 times and on the right 58 Downloaded from https://academic.oup.com/cz/article-abstract/64/3/351/4961447 by Ed 'DeepDyve' Gillespie user on 21 June 2018 Heubel Female competition alters mating preferences 355 times, v ¼ 1.507, P¼ 0.2195. Digital images of egg clutches were preferred to lay their eggs in the larger nest (with female competi- analyzed using Image J (Image J 1.43s public domain software tors: n ¼ 25, v ¼ 9.64, P ¼ 0.002; without female competitors Wayne Rasband, NIH, USA). Clutch size was analyzed as clutch n ¼ 43, v ¼ 15.49, P< 0.001; Table 1 and Figure 2A). There was no area (mm ) as the number of eggs is strongly linearly related to the difference in the mating propensity (i.e., the proportion of the likeli- clutch area (Heubel et al. 2008). As response variables I tested mating hood for mating to take place) between the 2 social contexts propensity (yes, no), mate choice (stimulus 1, stimulus 2), latency until (v ¼ 3.135, P ¼ 0.077; Table 1). spawning (min), and clutch size (mm ). Binary female mating deci- The latency until spawning did not differ between the 2 social contexts (with or without female competitors; F ¼ 0.137, sions were tested using nominal logistic models and log-likelihood 1,65 ratio tests. Continuous response variables (latency, clutch size) were P ¼ 0.712). The onset of spawning took longer in the smaller nest tested using linear models. I checked residual plots to confirm model [latency for small nests: 733 min6 146, for large nests: 4026 76 assumptions. For latency data, I initially also checked whether a log (mean6 SE); F ¼ 4.172, P ¼ 0.045]. There was no social con- 1,65 transformation would improve the models. In the male-size experi- text: nest size interaction and no effect by female body size, ment (2), 2 outliers (beyond 97.5 quantile) had to be excluded to meet Figure 2B). model assumptions when analyzing latencies. All linear models Clutch size was not affected by social context (F ¼ 1.034, 1,63 included 2 fixed factors to represent the experimental design: the social P ¼ 0.313) or nest size (F ¼ 0.279, P ¼ 0.599). There was no 1,63 context (female competition, control) and the mating partner (stimulus social context: nest size interaction. Larger females spawned more 1, stimulus 2). Using a model selection approach, I always started eggs (female total length F ¼ 21.431, P< 0.0001, slope estimate 1,63 b ¼ 27.026 5.84, Figure 2C). from an initial full model including as independent variables the 2 factors, all interactions, and female size as covariate. I then simplified models by iteratively removing interaction terms starting from the Male-size experiment (2) highest order terms and least significant terms. I compared models The mating propensity did not differ between the 2 social contexts with respect to minimize the Akaike Information Criteria (DAIC> 2) (v ¼ 0.067, P ¼ 0.796; Table 1). Females preferred large over small to obtain the best minimum adequate model. Non-significant males in the competition context. With female competitors present, (P> 0.05) covariates and interaction terms were only excluded from more than 75% of spawnings took place with the larger male the model if removal improved the model fit. Factors included as part (n ¼ 28, v ¼ 9.72, P¼ 0.002; Table 1 and Figure 3A). Without of the experimental design were never removed from the linear model. female competitors, females had no specific male size preference Statistical analyses were done using SAS JMP v. 13.0.0 ( 2016 SAS (n ¼ 25, v ¼ 0.04, P ¼ 0.841). There was a significant effect of the Institute Inc.) and R 3.3.1 (R Core Team 2016). social context treatment on whether or not females had a preference for larger males (log likelihood ratio test 2 2 table: n ¼ 53, v ¼ 4.21, P ¼ 0.040; Table 1 and Figure 3A). Results The latency until spawning did not differ between the 2 social Nest-size experiment (1) contexts (with or without female competitors; F ¼ 0.759, 1,47 More than 75% of spawnings took place in the larger nest. P ¼ 0.376; Figure 3B). Spawnings that took place with the larger Irrespective of presence or absence of female competitors, females male started sooner (3676 26 min) than trials in which females Table 1. Mating propensity and mating decisions for females in presence or absence of a perceived risk of female mating competition in 3 experiments testing female preferences for males differing in nest size (1), body size (2), or nest status (3) 2 2 Setup Treatment Mating v P Stimulus choice Stimulus 1 Stimulus 2 v P Experiment 1: Yes No Nest size Large nest Small nest nest size nn Control 46 27 4.94 0.026 N ¼43 34 9 15.49 <0.001 Competition 25 28 0.17 0.680 N ¼25 20 5 9.64 0.002 Nest size N ¼68 54 14 25.12 <0.001 Social effect* 3.14 0.077 N ¼68 0.01 0.927 Experiment 2: Yes No Male size Large male Small male male size Control 25 21 0.35 0.555 N ¼25 13 12 0.04 0.841 Competition 29 27 0.07 0.789 N ¼28 22 6 9.72 0.002 Male size N ¼53 35 18 5.55 0.018 Social effect* 0.07 0.796 N ¼53 4.21 0.040 Experiment 3: Yes No Nest status Already eggs Empty nest nest status in nest Control 11 6 1.47 0.225 N ¼11 4 7 0.81 0.366 Competition 20 1 17.19 <0.001 N ¼20 6 14 3.20 0.074 Nest status N ¼31 10 21 3.90 0.048 Social effect* 6.19 0.013 N¼31 0.13 0.718 Notes: Experiment 1: size-matched males. Experiment 2: size-matched nests. Experiment 3: size-matched males and size-matched nests. Both males had eggs;in1 randomly chosen nest earlier eggs were removed ¼ “empty nest”. *Social effect: log-likelihood ratio tests testing whether the probability of response is different across social contexts. P < 0.05 printed in bold. Downloaded from https://academic.oup.com/cz/article-abstract/64/3/351/4961447 by Ed 'DeepDyve' Gillespie user on 21 June 2018 356 Current Zoology, 2018, Vol. 64, No. 3 Figure 2. Nest-size experiment (1): testing female preferences for nest size. Figure 3. Male-size experiment (2): testing female preferences for male size. The 2 male stimuli were size-matched. (A) The number of observed spawning The 2 nests were size-matched. (A) The number of observed binary spawning decisions as binary outcomes with males in either the larger (black) or decisions with either the larger (black) or smaller (gray) male under the 2 dif- smaller (gray) nest under the 2 different social contexts, either with or without ferent social contexts, either with or without female competitors present in female competitors present in the adjacent compartment. (B) The time in the adjacent compartment. (B) The time in minutes (mean6 SE) until the minutes (mean6 SE) until the female spawned with 1 of the 2 males (in black female spawned with 1 of the 2 males (in black with the larger male, in gray matings with the male in the larger nest, in gray matings with the male in the with the smaller male). (C) The clutch area in mm (mean6 SE), the female smaller nest). (C) The clutch area in mm (mean6 SE), the female spawned spawned with the larger (black) or smaller (gray) male in the 2 different social with the male in the larger (black) or smaller (gray) nest in the 2 different contexts. social contexts. Downloaded from https://academic.oup.com/cz/article-abstract/64/3/351/4961447 by Ed 'DeepDyve' Gillespie user on 21 June 2018 Heubel Female competition alters mating preferences 357 Figure 5. The relationship between clutch size (mm ) and female total length (mm) across all 3 experiments and both social context treatment. Larger females spawned more eggs (r ¼ 0.31, y ¼ 30.07x713.76). Nest-status experiment (3) The mating propensity differed between the 2 social contexts (v ¼ 6.192, P ¼ 0.013; Table 1). There was a higher mating propen- sity in trials with female competitors present in the adjacent com- partment (95% in the competition treatment, 69% in the control treatment; Table 1). Sixty-eight percent of all spawnings occurred in the empty nest (nest status effect: n ¼ 31, v ¼ 3.90, P ¼ 0.048). The pattern of mating decisions did not differ depending on presence or absence of female competitors (social effect: log-likelihood ratio test, 2 2 table, n ¼ 31, v ¼ 0.13, P ¼ 0.718). Analyzing probabil- ities for mating with males in either empty nests or nests that already contain eggs for the 2 social contexts separately gives non- significant results (without female competitors 64% spawning in empty nest: n ¼ 11, v ¼ 0.81, P ¼ 0.366; with female competitors 70% spawning in empty nest: n ¼ 20, v ¼ 3.2, P ¼ 0.074; Table 1 and Figure 4A). The latency until spawning neither differed between the 2 social contexts (F ¼ 0.029, P ¼ 0.866) nor between empty nests and 1,27 those that already contained eggs (F ¼ 2.82, P ¼ 0.105). There 1,27 was no social context: nest size interaction and no effect by female body size (Figure 4B). Clutch size was not affected by social context (F ¼ 2.095, 1,26 Figure 4. Nest-status experiment (3): testing female preferences for nest sta- P ¼ 0.159) or nest status, that is whether nests were empty or tus. The 2 males and nests were size-matched. (A) The number of observed already contained eggs (F ¼ 2.026, P ¼ 0.166; Figure 4C).There 1,26 binary spawning decisions with the male in either the nest already with eggs was no social context: nest status treatment interaction. Larger (black) or the nest without eggs (gray) under the 2 different social contexts, either with or without female competitors present in the adjacent compart- females spawned more eggs (female total length as a covariate: ment. (B) The time in minutes (mean6 SE) until the female spawned with a F ¼ 8.259, P ¼ 0.008, slope estimate b ¼ 31.006 10.79). 1,26 male in 1 of the 2 nests (in black with eggs, in gray without eggs). (C) The Across all 3 experiments, larger females laid larger clutches clutch area in mm (mean6 SE), the female spawned with the male in the 2 (r ¼ 0.31, F ¼ 70.062, P< 0.001; Figure 5). This relationship 1,154 egg-containing nest (black) or the nest without eggs (gray) in the 2 different did not differ between the 3 experiments and was the same for social contexts. clutches laid in presence or absence of female competitors (Figure 5). There was no relationship between male properties (size, weight, condition factor) and clutch size or spawning latency. In mated with the smaller male (4626 35 min) (F ¼ 5.785, addition, neither spawning latency and egg number, nor male and 1,47 P ¼ 0.020). There was no social context: male size interaction and female size were correlated. no effect by female body size (Figure 3B). Clutch size was not affected by social context (F ¼ 0.033, 1,44 Discussion P ¼ 0.857) or male size (F ¼ 0.020, P ¼ 0.887, Figure 3C). There 1,44 was no social context: male size interaction. Larger females spawned Females had a general spawning preference for males in larger nests. more eggs (female total length as a covariate: F ¼ 26.975, In contrast, a preference for mating with larger males only occurred 1,44 P< 0.001, slope estimate b ¼ 33.526 6.45). under perceived female–female competition. Given a choice between Downloaded from https://academic.oup.com/cz/article-abstract/64/3/351/4961447 by Ed 'DeepDyve' Gillespie user on 21 June 2018 358 Current Zoology, 2018, Vol. 64, No. 3 males with nests that already contain eggs and those without eggs, careful mate choice decisions based on additional cues. Such behav- females rather spawn with the male in the empty nest and more so ior may aim at maximizing mate quality, paternal care performance, in the female-competitive context. Spawning latencies, the time it male competitive abilities, and reproductive success in a socially challenging environment in which males are expected to conduct took until mating, were shorter for matings with males in larger more demanding paternal care and nest defense duties. Larger com- nests and with larger males. The social context, more specifically the mon goby males and males in good condition are also better as perceived risk of female competition, had no effect on how long it intruders, by taking over other, smaller, males’ nests (Nyman 1953; took females to start spawning in any of the 3 experiments. Clutch Magnhagen 1992; Svensson and Forsgren 2003). In addition, size only depended on female size: larger females laid larger clutches. female–female competition may bear the risk of (too) many eggs The perceived risk of female competition did not affect how many inside nests leading to more demanding paternal care activities. eggs a female spawned. Interestingly, in the experiment offering Indeed, studies have shown that females prefer males that provide females a choice between males with nests that already contain eggs high levels of parental care (Forsgren 1997a; Ostlund and Ahnesjo ¨ versus males with empty nests, female competitors present in an 1998; Lindstro ¨ m et al. 2006). adjacent compartment led to a higher mating propensity and thus a Numerous examples show that reproductive behavior as a whole higher probability for females to decide to mate within a day. can be sensitive to the number and the sex of conspecifics [Heubel et al. 2008; Aronsen et al. 2013;see Kokko and Rankin (2006) for a Females prefer males with large nests review]. Especially for male body size, conflicting patterns and annual Studies on female mating preferences in the closely related sand goby fluctuations are known for female preferences in sand gobies Pomatoschistus minutus found similar preferences for larger and (Forsgren 1992, 1997a; Kvarnemo et al. 1995; Lehtonen et al. 2010). higher built nests (Svensson and Kvarnemo 2005; Lehtonen et al. As an example, females adjust their preferences according to the 2007). In absence of male competition, males selected their nests size- actual mating competition by a preference for larger males under assortatively (Kvarnemo 1995). However, not only as an indirect cue increased male mating competition (Lehtonen and Lindstro ¨m 2009). for the quality of the nest-holding male, also more directly are nests In competitive situations, larger males seem to be more likely to be also crucial resources required for reproduction, for which females able to maintain nests with many eggs. However, such context- should intensively compete (Clutton-Brock 2009). Females can and dependent flexibility of mating preferences can go in either direction. should use information on nest size and quality as an indicator of indi- Indeed, females do not always commence preferences for larger stim- rect or direct benefits if this renders a reliable cue of quality and gained uli. In Pomatoschistus marmoratus, females preferred the smaller resource benefits are sufficiently grand (Kokko 1998). Indeed, larger male and did not care about nest size when male–male competition common goby males are better at competing for large nest sites and was experimentally excluded (Locatello et al. 2016). In two-spotted nest maintenance and thus have more eggs in their nests than smaller gobies Gobiusculus flavescens and annual killifish (Austrolebias reich- males (Magnhagen and Vestergaard 1993). The observed clear prefer- erti, Rivulidae), early during the reproductive season, when the OSR ence for larger nests—both in terms of where to lay the eggs and how was still male-biased or even and female competition was weak, fast to decide whom to mate with—in the nest-size experiment (1) sug- females preferred larger males. Later, toward the end of the season gests that nest size may be a reliable and easy to evaluate indicator of under female-biased sex ratios and stronger female-competition, mate quality in common gobies. I initially also aimed at testing female females lost their size-related male preference (two-spotted goby: Borg preferences for male size and nest size in mismatched and matched et al. 2006; annual killifish: Passos et al. 2014). Such pattern rather combinations. However, whenever I staged asymmetric trials with supports the hypothesis of compromised low cost mating decisions small males in larger nests and larger males in smaller nests, both targeted at securing immediate mating success (Heubel et al. 2008). males swapped nests prior to mating (unpublished data) hinting at Thus, the specific nature of a change in the context seems to be rele- potentially male–male interactions reliably solving nest selection vant for whether a cue may be added or dropped in mate assessment. among males prior to mating (Japoshvili et al. 2012). Lehtonen et al. (2007) used a similar setup showing a female association preferences Females prefer to spawn with males in empty nests for the larger males in the larger nests. Thus, the nest could be consid- In various species with paternal care, females prefer to add their ered to be a part of the male’s extended phenotype (Dawkins 1982; eggs into nests that already contain eggs (reviewed in Forsgren et al. Schaedelin and Taborsky 2006). However, the relationship between 1996a). Such behavior can be explained by the presence of eggs male body condition and nest attributes may be unstable and thus directly indicating good parenting skills (Sargent 1988; Kraak and under certain conditions, females should rather rely on multiple cues van den Berghe 1992), dilution effects (Ridley and Rechten 1981; formatechoice(Candolin 2003; Lehtonen and Wong 2009). Unger and Sargent 1988), mate choice-copying (Dugatkin 1992; Gibson and Ho ¨ glund 1992; Pruett-Jones 1992), increased hatching Social context matters: females use male size as success with increasing brood size due to lowered filial cannibalism additional cue (Rohwer 1978), and expected higher paternal investment in larger One such additional cue may be directly assessing male size upon and more valuable clutches (Coleman et al. 1985; Sargent 1988; female mate choice decisions in situations when nests appear equally Petersen and Marchetti 1989; Vallon and Heubel 2017). large. Interestingly, in the current study, females expressed a prefer- Alternatively, females may prefer males with empty nests or nests ence for mating with larger males only when female competitors that only contain fewer eggs to avoid being the last (Andre ´ n and were present. A situation with an excess of females may at the same Kvarnemo 2014). The last added clutch bears the highest risk of fil- time be perceived as a shortage of nests and mating opportunities. ial cannibalism (Salfert and Moodie 1985; Petersen and Marchetti Hayes et al. (2016) found similar results for female fiddler crabs 1989; Klug and Lindstro ¨ m 2008; Vallon and Heubel 2016). This exhibiting stronger preferences for larger claws under female biased alternative view is especially relevant for common gobies as a species conditions. This pattern of an emerging preference for larger males with naturally limited space for eggs in their nest (Pampoulie et al. in a female-competitive situation supports my hypothesis of more 2001; Mu ¨ ck and Heubel 2018) and selective filial cannibalism Downloaded from https://academic.oup.com/cz/article-abstract/64/3/351/4961447 by Ed 'DeepDyve' Gillespie user on 21 June 2018 Heubel Female competition alters mating preferences 359 targeted at the youngest, last added clutch (Vallon and Heubel their mating preferences in a choice situation under different per- 2016). Here, the nest-status experiment (3) showed a clear female ceived risks of female mating competition. In nature, nest attributes preference for males with empty nests in a system where a second, and male attributes may usually be linked and appear as a hierarchi- added clutch would most likely be the last one of a brood for the cal suite of easily accessible and more difficult but more reliable cues current reproductive cycle. to evaluate mates. The results of this study emphasize that common goby females are sensitive to the presence of a female audience, imposing female mate-competition when choosing a mate. In addi- Mate sampling and female investment tion to nest size as a generally preferred and easily assessable attrib- In an earlier study with females making mating decisions in a no- ute of a male, females also rely on male body size as an additional choice situation in a female-competitive environment, females more subtle cue for mate quality in the presence of additional spawned faster and more eggs [Heubel et al. 2008, but see also females. Myint et al. (2011) for the opposite pattern in another goby species, Rhinogobius flumineus]. In contrast, here I found clear differences in spawning latencies with respect to the choice of male traits but no Acknowledgments difference in spawning latency or clutch size when competitors were I thank Johanna Eklund, Mirka Heinonen, Simo Rintakoski, and Eeva present or absent. Spawning latency is a good proxy for a females’ Soininen for assistance with experiments and help in the ﬁeld, Phillip Gienapp willingness to mate with a specific mate (Lindstro ¨ m and Kangas for continuous logistic support during ﬁeld work, and Kai Lindstro ¨ m and 1996). Prolonged latencies may reflect either a degree of reluctance Hanna Kokko for continuous support throughout the entire study, and 2 to mate or be a sign of extended mate sampling (Lindstro ¨ m and anonymous referees for commenting on an earlier version of the manuscript. Lehtonen 2013). In a field study on mate sampling in two-spotted Tva ¨ rminne Zoological Station provided excellent working facilities. This gobies in a population with a known seasonal shift toward elevated research adhered to the Association for the Study of Animal Behaviour female competition, females became less choosy and visited fewer Guidelines for the Use of Animals in Research and the legal requirements of males later during the reproductive season (Myhre et al. 2012). Finland. All procedures were approved by the animal care committee of the A similar study on sand gobies, however, showed the reversed tempo- University of Helsinki and declared as class 0 experiments and inspected and approved by ELLA, Animal Experimental Board in Finland on site at ral shift toward intensified mate sampling later in the season Tva ¨ rminne zoological station in Hanko, Finland. Research and sampling of (Forsgren 1997b). Such longer mate sampling intervals may for ﬁsh permitted with decisions no. 1605, 26833/33/78Fa Ros, no. 1769, 14810 example arise if females take more time evaluating potential mates in 361 83 Y Tva ¨ issued by Uudenmaan La¨a ¨ nihallitus, Finland. situations where mate choice cues reveal ambiguous messages such as the male evaluated as being of higher quality residing in the smaller nest, or the smaller male having built the more elaborate nest. In the Funding current study, spawning latencies were longer for matings that ended Funding was provided by the Academy of Finland (project 117398) and the up with the smaller male and with males in the smaller nest, the gen- Volkswagen Foundation (project 84 846, 92 002). The author declares no erally less preferred phenotype. Here, latency or mate sampling conﬂict of interest. depended on male cues, not on the female competitive context. At first sight, this is surprising as Heubel et al. 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