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1.  The influence of recent social experience and physical environment on courtship and male aggression 
Social and environmental factors can profoundly impact an individual’s investment of resources into different components of reproduction. Such allocation trade-offs are expected to be amplified under challenging environmental conditions. To test these predictions, we used a desert-dwelling fish, the desert goby, Chlamydogobius eremius, to experimentally investigate the effects of prior social experience (with either a male or a female) on male investment in courtship and aggression under physiologically benign and challenging conditions (i.e., low versus high salinity).
We found that males maintained a higher level of aggression towards a rival after a recent encounter with a female, compared to an encounter with a male, under low (but not high) salinity. In contrast, male investment in courtship behaviour was unaffected by either salinity or social experience.
Together, our results suggest that male investment in aggression and courtship displays can differ in their sensitivity to environmental conditions and that not all reproductive behaviours are similarly influenced by the same environmental context.
PMCID: PMC4721148  PMID: 26792425
Aggression; Behavioural plasticity; Courtship display; Encounter rate; Environmental effect; Physiological cost; Salinity; Sexual signal; Social experience
2.  Allopatry, competitor recognition and heterospecific aggression in crater lake cichlids 
Aggressive behaviour can have significant evolutionary consequences–not only within species, but also in the context of heterospecific interactions. Here, we carried out an experimental field study to investigate the importance of phenotypic similarity on levels of aggression between species whilst controlling for familiarity effects using manipulated allopatric stimuli. Specifically, we investigated aggressive responses of territory holding males and females in two species of Neotropical cichlid fish, Amphilophus sagittae and Hypsophrys nicaraguensis, that differ in their phenotypic similarity to our allopatric stimulus species, Amphilophus astorquii.
We found that, independent of phenotypic similarity (and correlated phylogenetic proximity) between the territory holders and intruder, territorial aggression was not adjusted in relation to allopatric intruder colour markings that are associated with different levels of threat and known to provoke different responses in a sympatric setting. We also found that males and females did not differ in their overall patterns of aggression adjustment towards intruder cues. Nevertheless, the two focal species, which share the same breeding grounds and external threats, exhibited different sex roles in breeding territory defence.
Together with earlier studies assessing hetrospecific aggression in sympatry, our current results highlight the importance of coevolution and learning in species interactions.
PMCID: PMC4700676  PMID: 26729482
Allopatry; Behavioural plasticity; Cichlid fish; Colour signal; Competitor recognition; Heterospecific aggression; Phenotypic similarity; Signal reliability; Species interaction
4.  Effects of salinity on nest-building behaviour in a marine fish 
BMC Ecology  2016;16:7.
Parental allocation and reproductive success are often strongly influenced by environmental factors. In this respect, salinity is a key factor influencing species distributions and community structure in aquatic animals. Nevertheless, the effects of salinity on reproductive behaviours are not well known. Here, we used the sand goby (Pomatoschistus minutus), a small fish inhabiting a range of different salinities, to experimentally assess the effects of changes in salinity on nesting behaviour, a key component of reproduction in sand gobies and many other taxa.
We found that salinity levels influenced some aspects of male nesting behaviour (i.e. nest entrance size) but not others (i.e. latency to build a nest, choice of nest site, sand on top of nest) and that small and large individuals were differently affected. In particular, the importance of body size in adjustment of nest entrance depended on the salinity level.
The results support the prediction that geographically widespread aquatic species, such as sand gobies, are able to perform well under a range of salinity levels. The phenotype by environment interaction found between male size and behavioural responses to salinity can, in turn, help to explain the notable variation observed in nest-building (and other) behaviours closely linked to reproduction.
Electronic supplementary material
The online version of this article (doi:10.1186/s12898-016-0067-y) contains supplementary material, which is available to authorized users.
PMCID: PMC4772348  PMID: 26928449
Body size; Environmental change; Nest-building; Parental care; Phenotypic plasticity; Salinity; Sand goby
5.  Mate sampling and choosiness in the sand goby 
To date, mate choice studies have mostly focused on establishing which mates are chosen or how the choices are performed. Here, we combined these two approaches by empirically testing how latency to mate is affected by various search costs, variation in mate quality and female quality in the sand goby (Pomatoschistus minutus). Our results show that females adjust their mating behaviour according to the costs and benefits of the choice situation. Specifically, they mated sooner when access to males was delayed and when the presence of other females presented a mate sampling cost. We also found a positive link between size variation among potential mating partners and spawning delay in some (but not all) experimental conditions. By contrast, we did not find the number of available males or the females' own body size (‘quality’) to affect mating latency. Finally, female mating behaviour varied significantly between years. These findings are notable for demonstrating that (i) mate sampling time is particularly sensitive to costs and, to a lesser degree, to variation among mate candidates, (ii) females' mating behaviour is sensitive to qualitative rather than to quantitative variation in their environment, and (iii) a snapshot view may describe mate sampling behaviour unreliably.
PMCID: PMC3712446  PMID: 23804620
mate choice; mate searching; mating strategy; sampling cost; sexual selection; time constraint
6.  A High Aggression Strategy for Smaller Males 
PLoS ONE  2012;7(8):e43121.
Male-male conflict is common among animals, but questions remain as to when, how and by whom aggression should be initiated. Factors that affect agonistic strategies include residency, the value of the contested resource and the fighting ability of the two contestants. We quantified initiation of aggression in a fish, the desert goby, Chlamydogobius eremius, by exposing nest-holding males to a male intruder. The perceived value of the resource (the nest) was manipulated by exposing half of the residents to sexually receptive females for two days before the trial. Resident male aggression, however, was unaffected by perceived mating opportunities. It was also unaffected by the absolute and relative size of the intruder. Instead resident aggression was negatively related to resident male size. In particular, smaller residents attacked sooner and with greater intensity compared to larger residents. These results suggest that resident desert goby males used set, rather than conditional, strategies for initiating aggression. If intruders are more likely to flee than retaliate, small males may benefit from attacking intruders before these have had an opportunity to assess the resident and/or the resource.
PMCID: PMC3419218  PMID: 22905213
7.  Heritability and adaptive significance of the number of egg-dummies in the cichlid fish Astatotilapia burtoni 
Cichlid fishes are a textbook example of rapid speciation and exuberant diversity—this applies especially to haplochromines, a lineage with approximately 1800 species. Haplochromine males uniquely possess oval, bright spots on their anal fin, called ‘egg-spots’ or ‘egg-dummies’. These are presumed to be an evolutionary key innovation that contributed to the tribe's evolutionary success. Egg-spots have been proposed to mimic the ova of the mouthbrooding females of the corresponding species, contribute to fertilization success and even facilitate species recognition. Interestingly, egg-spot number varies extensively not only between species, but also within some populations. This high degree of intraspecific variation may appear to be counterintuitive since selection might be expected to act to stabilize traits that are correlated with fitness measures. We addressed this ‘paradox’ experimentally, and found that in the haplochromine cichlid Astatotilapia burtoni, the number of egg-spots was related to male age, body condition and dominance status. Intriguingly, the egg-spot number also had a high heritable component (narrow sense heritability of 0.5). These results suggest that the function of egg-spots might have less to do with fertilization success or species recognition, but rather relate to mate choice and/or male–male competition, helping to explain the high variability in this important trait.
PMCID: PMC3119019  PMID: 21208958
body condition; dominance hierarchy; narrow sense heritability; intraspecific variation; key innovation; signal value
8.  Introduced Predator Elicits Deficient Brood Defence Behaviour in a Crater Lake Fish 
PLoS ONE  2012;7(1):e30064.
Introduced species represent one of the most serious global threats to biodiversity. In this field-based study, we assessed behavioural responses of brood tending cichlid fish to an invasive predator of their offspring. This was achieved by comparing parental defence responses of the endangered arrow cichlid (Amphilophus zaliosus), a fish species endemic to the crater lake Apoyo in Nicaragua, towards the bigmouth sleeper (Gobiomorus dormitor), a formidable predator of cichlid fry, and all other potential fish predators of offspring. The bigmouth sleeper was recently introduced into Apoyo but naturally co-exists with cichlids in a few other Nicaraguan lakes. Arrow cichlid parents allowed bigmouth sleepers to advance much closer to their fry than other predators before initiating aggressive brood defence behaviours. Interestingly, parents of a very closely related species, A. sagittae, which has coevolved with bigmouth sleepers in crater lake Xiloá, reacted to approaching bigmouth sleepers at comparable distances as to other predators of cichlid fry. These results provide a novel demonstration of the specific mechanism (i.e. naive parental behaviour) by which invasive predators may negatively affect species that lack the adequate behavioural repertoire.
PMCID: PMC3253807  PMID: 22253881
9.  Both male and female identity influence variation in male signalling effort 
Male sexual displays play an important role in sexual selection by affecting reproductive success. However, for such displays to be useful for female mate choice, courtship should vary more among than within individual males. In this regard, a potentially important source of within male variation is adjustment of male courtship effort in response to female traits. Accordingly, we set out to dissect sources of variation in male courtship effort in a fish, the desert goby (Chlamydogobius eremius). We did so by designing an experiment that allowed simultaneous estimation of within and between male variation in courtship, while also assessing the importance of the males and females as sources of courtship variation.
Although males adjusted their courtship depending on the identity of the female (a potentially important source of within-male variation), among-male differences were considerably greater. In addition, male courtship effort towards a pair of females was highly repeatable over a short time frame.
Despite the plasticity in male courtship effort, courtship displays had the potential to reliably convey information about the male to mate-searching females. Our experiment therefore underscores the importance of addressing the different sources contributing to variation in the expression of sexually-selected traits.
PMCID: PMC3163561  PMID: 21827657
10.  Local variation and parallel evolution: morphological and genetic diversity across a species complex of neotropical crater lake cichlid fishes 
The polychromatic and trophically polymorphic Midas cichlid fish species complex (Amphilophus cf. citrinellus) is an excellent model system for studying the mechanisms of speciation and patterns of phenotypic diversification in allopatry and in sympatry. Here, we first review research to date on the species complex and the geological history of its habitat. We analyse body shape variation from all currently described species in the complex, sampled from six crater lakes (maximally 1.2–23.9 kyr old) and both great lakes in Nicaragua. We find that Midas cichlid populations in each lake have their own characteristic body shape. In lakes with multiple sympatric species of Midas cichlid, each species has a distinct body shape. Across the species complex, most body shape change relates to body depth, head, snout and mouth shape and caudal peduncle length. There is independent parallel evolution of an elongate limnetic species in at least two crater lakes. Mitochondrial genetic diversity is higher in crater lakes with multiple species. Midas cichlid species richness increases with the size and age of the crater lakes, though no such relationship exists for the other syntopic fishes. We suggest that crater lake Midas cichlids follow the predicted pattern of an adaptive radiation, with early divergence of each crater lake colonization, followed by intralacustrine diversification and speciation by ecological adaptation and sexual selection.
PMCID: PMC2871887  PMID: 20439280
geometric morphometrics; mitochondrial DNA genetic diversity; ecomorphology; limnology; Mesoamerica; adaptive radiation
11.  Fluctuating mate preferences in a marine fish 
Biology Letters  2009;6(1):21-23.
According to theory, directional female choice for male sexual ornaments is expected to erode underlying genetic variation. Considerable attention, in this regard, has been given to understanding the ubiquity of heritable genetic variation in both female choice and male sexual traits. One intriguing possibility emerging from this work is that persistent genetic variation could be maintained, over time, by variation in female mate preferences. Here, we report the results of a four-year study showing significant year-to-year fluctuations in mate preferences in a small marine fish, the sand goby, Pomatoschistus minutus. Although the average size of mature fish varied across years, we were unable to find direct evidence linking this variation to differences in female preferences among years. Our results, nevertheless, underscore the importance of temporal fluctuations in female mate preferences, as these can have important consequences for understanding variation in sexual traits and the intensity of sexual selection.
PMCID: PMC2817248  PMID: 19675000
body size; lek paradox; mate choice; sand goby; sexual selection; temporal fluctuation
12.  Rapid sympatric ecological differentiation of crater lake cichlid fishes within historic times 
BMC Biology  2010;8:60.
After a volcano erupts, a lake may form in the cooled crater and become an isolated aquatic ecosystem. This makes fishes in crater lakes informative for understanding sympatric evolution and ecological diversification in barren environments. From a geological and limnological perspective, such research offers insight about the process of crater lake ecosystem establishment and speciation. In the present study we use genetic and coalescence approaches to infer the colonization history of Midas cichlid fishes (Amphilophus cf. citrinellus) that inhabit a very young crater lake in Nicaragua-the ca. 1800 year-old Lake Apoyeque. This lake holds two sympatric, endemic morphs of Midas cichlid: one with large, hypertrophied lips (~20% of the total population) and another with thin lips. Here we test the associated ecological, morphological and genetic diversification of these two morphs and their potential to represent incipient speciation.
Gene coalescence analyses [11 microsatellite loci and mitochondrial DNA (mtDNA) sequences] suggest that crater lake Apoyeque was colonized in a single event from the large neighbouring great lake Managua only about 100 years ago. This founding in historic times is also reflected in the extremely low nuclear and mitochondrial genetic diversity in Apoyeque. We found that sympatric adult thin- and thick-lipped fishes occupy distinct ecological trophic niches. Diet, body shape, head width, pharyngeal jaw size and shape and stable isotope values all differ significantly between the two lip-morphs. The eco-morphological features pharyngeal jaw shape, body shape, stomach contents and stable isotopes (δ15N) all show a bimodal distribution of traits, which is compatible with the expectations of an initial stage of ecological speciation under disruptive selection. Genetic differentiation between the thin- and thick-lipped population is weak at mtDNA sequence (FST = 0.018) and absent at nuclear microsatellite loci (FST < 0.001).
This study provides empirical evidence of eco-morphological differentiation occurring very quickly after the colonization of a new and vacant habitat. Exceptionally low levels of neutral genetic diversity and inference from coalescence indicates that the Midas cichlid population in Apoyeque is much younger (ca. 100 years or generations old) than the crater itself (ca. 1 800 years old). This suggests either that the crater remained empty for many hundreds of years after its formation or that remnant volcanic activity prevented the establishment of a stable fish population during the early life of the crater lake. Based on our findings of eco-morphological variation in the Apoyeque Midas cichlids, and known patterns of adaptation in Midas cichlids in general, we suggest that this population may be in a very early stage of speciation (incipient species), promoted by disruptive selection and ecological diversification.
PMCID: PMC2880021  PMID: 20459869
13.  Convict cichlids benefit from close proximity to another species of cichlid fish 
Biology Letters  2008;4(6):610-612.
The coexistence of species with overlapping resource use is often thought to involve only negative fitness effects as a consequence of interspecific competition. Furthermore, the scarce empirical research on positive species interactions has predominantly focused on sessile organisms. Here, I experimentally assessed the effect of close proximity of a potential brood predator and competitor on reproductive success of a neotropical cichlid fish. I demonstrate that convict cichlid (Archocentrus nigrofasciatus) broods have a higher survival rate near territories of the Nicaragua cichlid (Hypsophrys nicaraguensis), and that escape from predation and nest takeovers is the most likely explanation for the decreased offspring mortality.
PMCID: PMC2614157  PMID: 18762472
facilitation; offspring survival; positive interspecific interaction; predation avoidance; species coexistence

Results 1-13 (13)