Sigal Balshine

Female promiscuity promotes the evolution of faster sperm in cichlid fishes

Sperm competition, the contest among ejaculates from rival males to fertilize ova of a female, is a common and powerful evolutionary force influencing ejaculate traits. During competitive interactions between ejaculates, longer and faster spermatozoa are expected to have an edge; however, to date, there has been mixed support for this key prediction from sperm competition theory. Here, we use the spectacular radiation of cichlid fishes from Lake Tanganyika to examine sperm characteristics in 29 closely related species. We provide phylogenetically robust evidence that species experiencing greater levels of sperm competition have faster-swimming sperm. We also show that sperm competition selects for increases in the number, size, and longevity of spermatozoa in the ejaculate of a male, and, contrary to expectations from theory, we find no evidence of trade-offs among sperm traits in an interspecific analysis. Also, sperm swimming speed is positively correlated with sperm length among, but not within, species. These different responses to sperm competition at intra- and interspecific levels provide a simple, powerful explanation for equivocal results from previous studies. Using phylogenetic analyses, we also reconstructed the probable evolutionary route of trait evolution in this taxon, and show that, in response to increases in the magnitude of sperm competition, the evolution of sperm traits in this clade began with the evolution of faster (thus, more competitive) sperm.

Correlates of group size in a cooperatively breeding cichlid fish (Neolamprologus pulcher)

Abstract. Neolamprologus pulcher, a cooperatively breeding cichlid fish from Lake Tanganyika, lives in permanent social groups comprising one breeding pair and helpers of both sexes. Variation in group size (1–14 helpers) provides an opportunity to investigate factors that affect how many helpers remain in a group and in turn how group size affects reproductive success. This field study showed that larger groups live in larger territories with more shelter. Group size was more strongly correlated with territory quality than with breeder size. Experimental enhancement of territory quality did not affect group size but group size decreased when territory quality was reduced. Breeders living in a large group benefit because such individuals feed more often and have lower workloads and greater reproductive success. Helpers in larger groups also fed more frequently but did not have lower workloads. This is one of the first experimental studies to examine the factors influencing group size in cooperative breeders.

Relatedness and helping in fish: examining the theoretical predictions

Many studies have attempted to explain the evolution of cooperation, yet little attention has been paid to what factors control the amount or kind of cooperation performed. Kin selection theory suggests that more cooperation, or help, should be given by relatives. However, recent theory suggests that under specific ecological and demographic conditions, unrelated individuals must ‘pay to stay’ in the group and therefore may help more. We tested these contrasting predictions using the cooperatively breeding fish, Neolamprologus pulcher, and found that the degree of work effort by helpers depended on which helping behaviours were considered and on their level of relatedness to the breeding male or female. In the field, helpers unrelated to the breeding male performed more territory defence, while helpers unrelated to the breeding female contributed less to territory defence. In the laboratory, unrelated group members helped more. Our work demonstrates that a number of factors in addition to kinship shape cooperative investment patterns.

Competitive Interactions between Round Gobies and Logperch

We examined territorial defense and behavioural interactions between two species of fish resident in Hamilton Harbour: non-indigenous round gobies (Neogobius melanostomus) and native logperch (Percina caprodes). Trials consisted of placing one fish, “the resident” (either a round goby or a logperch), in a tank with a shelter for 24 hours before adding another fish, “the intruder” (either a round goby or a logperch), and recording aggressive incidents. Overall, gobies exhibited more aggressive behavior than logperch, and in general resident status had no effect on amount of aggression displayed. Also, gobies spent more time in shelters than logperch, and overall resident status did not affect the amount of time spent under shelter. We also compared abundance data for gobies and logperch using electrofishing transects in Hamilton Harbour that were conducted in 1995 and 2001 and found a dramatic increase in round goby numbers and a non-significant decrease in logperch numbers. Our data suggest that gobies are superior space competitors and hence the range expansion coupled with an increasing population size of the round gobies in Hamilton Harbour is likely to have deleterious consequences for logperch populations.

The evolution of cooperative breeding in the African cichlid fish, Neolamprologus pulcher.

The conundrum of why subordinate individuals assist dominants at the expense of their own direct reproduction has received much theoretical and empirical attention over the last 50 years. During this time, birds and mammals have taken centre stage as model vertebrate systems for exploring why helpers help. However, fish have great potential for enhancing our understanding of the generality and adaptiveness of helping behaviour because of the ease with which they can be experimentally manipulated under controlled laboratory and field conditions. In particular, the freshwater African cichlid, Neolamprologus pulcher, has emerged as a promising model species for investigating the evolution of cooperative breeding, with 64 papers published on this species over the past 27 years. Here we clarify current knowledge pertaining to the costs and benefits of helping in N. pulcher by critically assessing the existing empirical evidence. We then provide a comprehensive examination of the evidence pertaining to four key hypotheses for why helpers might help: (1) kin selection; (2) pay‐to‐stay; (3) signals of prestige; and (4) group augmentation. For each hypothesis, we outline the underlying theory, address the appropriateness of N. pulcher as a model species and describe the key predictions and associated empirical tests. For N. pulcher, we demonstrate that the kin selection and group augmentation hypotheses have received partial support. One of the key predictions of the pay‐to‐stay hypothesis has failed to receive any support despite numerous laboratory and field studies; thus as it stands, the evidence for this hypothesis is weak. There have been no empirical investigations addressing the key predictions of the signals of prestige hypothesis. By outlining the key predictions of the various hypotheses, and highlighting how many of these remain to be tested explicitly, our review can be regarded as a roadmap in which potential paths for future empirical research into the evolution of cooperative breeding are proposed. Overall, we clarify what is currently known about cooperative breeding in N. pulcher, address discrepancies among studies, caution against incorrect inferences that have been drawn over the years and suggest promising avenues for future research in fishes and other taxonomic groups.

Masculinized dominant females in a cooperatively breeding species

The molecular mechanisms underlying complex social behaviours such as dominance are largely unknown. Studying the cooperatively breeding African cichlid Neolamprologus pulcher, we show that dominant females were similar to dominant males in dominance behaviour, high testosterone levels and brain arginine vasotocin expression (a neuropeptide involved in vertebrate territorial, reproductive and social behaviours) compared to subordinate helpers, but had lower levels of 11‐ketotestosterone than males. Furthermore, brain gene expression profiles of dominant females were most similar to those of the males (independent of social rank). Dominant breeder females are masculinized at the molecular and hormonal level while being at the same time reproductively competent, suggesting a modular organization of molecular and endocrine functions, allowing for sex‐specific regulation.

Sex differences in rates of territory joining and inheritance in a cooperatively breeding cichlid fish

In social groups, subordinates may gain dominant breeding status either by inheriting the top position in their current group or by dispersing to join a new group. The pathway to breeder status is likely to vary between males and females as a result of sex differences in the costs of dispersal and inbreeding. We report results from a field study conducted to explore sex differences in the rates of territory joining and inheritance in a cooperatively breeding cichlid, Neolamprologus pulcher. We experimentally created 34 breeding vacancies and investigated the effects of breeder removal on the degree of cooperative behaviour and how changes in status influenced reproductive physiology. We found that 71% of male vacancies were filled by joiners (incoming fish, not previously members of the group) entering the territory. In contrast, only 15% of female vacancies were filled by joiners entering the group from elsewhere. Helpers increased their frequency of cooperative behaviour following the removal of a female breeder, but not following removal of a male breeder. Our results suggest that female breeder vacancies are typically filled by subordinate helpers who inherit from within the group and that male breeder vacancies are commonly filled by joining individuals (existing breeders or former helpers from other groups). Male social status and gonadal investment were positively correlated. This study represents one of the first experimental attempts to examine sexual differences in the pathway to breeding status in a cooperatively breeding species.

Androgens and dominance: Sex-specific patterns in a highly social fish (Neolamprologus pulcher)

In most vertebrates, aggression and dominance are tightly linked to circulating testosterone. Fish, however, have two androgens (testosterone, T and 11-ketotestosterone, 11KT) that influence aggression and dominance. To date, few studies have compared the relationship between androgen levels and the outcome of aggressive contests in both females and males of the same species. To investigate sex differences in androgens we staged size-matched, limited-resource (territory) contests with 14 female-female and 10 male-male pairs of the highly social cichlid Neolamprologus pulcher. We then examined androgen levels in recently established dominants, who won the contest and subsequently acquired a territory (for 3h), and subordinates, who lost and did not acquire a territory. Newly dominant females had higher plasma T but similar 11KT levels to newly subordinate females. In contrast, newly dominant males had higher 11KT but similar T levels to subordinate males. The ratio of 11KT to T, which demonstrates physiological importance of T conversion to 11KT, was positively correlated with submissive behavior in female winners, and correlated weakly with aggressive behavior in male winners (p=0.05). These findings provide support for the hypothesis that different androgens play equivalent roles in female versus male dominance establishment, and suggest that relative levels of 11KT and T are implicated in female dominance behavior and perhaps behavior of both sexes.

Demography and substrate affinity of the round goby (Neogobius melanostomus) in Hamilton Harbour

ABSTRACT The invasive round goby, Neogobius melanostomus, consumes eggs and fry of other fishes, competes for resources with native fish species, and hence poses a threat to Great Lakes aquatic communities. We provide the first description of round goby demographic patterns in Hamilton Harbour, in the western tip of Lake Ontario, and the connected Cootes Paradise Marsh, a recently restored wetland. By monitoring round goby populations on a variety of distinct habitats for 7 years (2002–2008), we found that populations have declined at all sample locations and that average fish body size also has decreased. We also related abundance, body size, and reproductive patterns to seasonality, to substrate types (mud, sand, cobble and boulder) and to water quality in all locations. Round gobies were found on all substrates sampled including mud, although they were less abundant on mud than on other substrates, and to date have not extensively colonized Cootes Paradise Marsh. Our work confirms previous studies, which have suggested that habitats lacking hard structures will have fewer round gobies because they lack substrates on which round gobies can breed. However, our results also indicate that muddy and sandy substrates are not resistant to round goby invasion and will not prevent round goby colonization, a potential concern for Cootes Paradise Marsh an important spawning, nursery, and refuge habitat for warmwater native fishes and for other similar wetlands.

Reproductive-Tactic-Specific Variation in Sperm Swimming Speeds in a Shell-Brooding Cichlid

Abstract Theory predicts that males experiencing elevated levels of sperm competition will invest more in gonads and produce faster-swimming sperm. Although there is ample evidence in support of the first prediction, few studies have examined sperm swimming speed in relation to sperm competition. In this study, we tested these predictions from sperm competition theory by examining sperm characteristics in Telmatochromis vittatus, a small shell-brooding cichlid fish endemic to Lake Tanganyika. Males exhibit four different reproductive tactics: pirate, territorial, satellite, and sneaker. Pirate males temporarily displace all other competing males from a shell nest, whereas sneaker males always release sperm in the presence of territorial and satellite males. Due to the fact that sneakers spawn in the presence of another male, sneakers face the highest levels of sperm competition and pirates the lowest, whereas satellites and territorials experience intermediate levels. In accordance with predictions, sperm from sneakers swam faster than sperm from males adopting the other reproductive tactics, whereas sperm from pirates was slowest. Interestingly, we were unable to detect any variation in sperm tail length among these reproductive tactics. Thus, sperm competition appears to have influenced sperm energetics in this species without having any influence on sperm size.