Sex ratios deviate across killifish species without clear links to life history

Sex ratios can differ from an expected equal proportion of males and females, carrying substantial implications for our understanding of how mating systems evolve. Typically, macro-evolutionary studies have been conducted without assessing how deviations from an equal sex ratio could be explained by sex-biased mortality or dispersal. Our understanding of sex ratio evolution independent of these confounds, in addition to any putative links between skewed sex ratios and other factors (e.g. life history), therefore remains largely unexplored. Here, we conducted an exploratory study investigating differences in sex ratios across closely related species while controlling for extrinsic mortality. We also tested two factors, non-overlapping/overlapping generations and the social environment, which have both been hypothesised to affect sex ratios. Specifically, we raised 15 species of killifish, which have either overlapping or discrete generations, under both solitary and social treatments. We found substantial divergences in sex ratios across closely related species, which exhibited both male and female biases. In conjunction with a low phylogenetic signal, our results suggest that sex ratios can evolve rapidly in this group. However, we found no evidence that overlapping generations or the social environment affected sex biases, suggesting that other factors drive the rapid evolution of sex ratios in killifishes

Fast life-histories are associated with larger brain size in killifishes

The high energetic demands associated with the vertebrate brain are proposed to result in a trade-off between the pace of life-history and relative brain size. However, because both life-history and brain size also have a strong relationship with body size, any associations between the pace of life-history and relative brain size may be confounded by coevolution with body size. Studies on systems where contrasts in the pace of life-history occur without concordant contrasts in body size could therefore add to our understanding of the potential coevolution between relative brain size and life-history. Using one such system - 21 species of killifish - we employed a common garden design across two ontogenetic stages to investigate the association between relative brain size and the pace of life-history. Contrary to predictions, we found that relative brain size was larger in adult fast-living killifishes, compared to slow-living species. Although we found no differences in relative brain size between juvenile killifishes. Our results suggest that fast- and slow-living killifishes do not exhibit the predicted trade-off between brain size and life-history. Instead, fast and slow-living killifishes could differ in the ontogenetic timing of somatic versus neural growth or inhabit environments that differ considerably in cognitive demands

Macroevolutionary evidence suggests trait-dependent coevolution between behavior and life-history

ABSTRACT Species with fast life-histories typically prioritize current over future reproductive events, compared to species with slow life-histories. These species therefore require greater energetic input into reproduction, and also likely have less time to realize their reproductive potential. Hence, behaviours that increase access to both resources and mating opportunities, at a cost of increased mortality risk, could coevolve with the pace of life-history. However, whether this prediction holds across species, remains untested under standardized conditions. Here, we test how risky behaviours, which facilitate access to resources and mating opportunities (i.e. activity, boldness and aggression), along with metabolic rate, coevolve with the pace of life-history across 20 species of killifish that present remarkable divergences in the pace of life-history. We found a positive association between the pace of life-history and aggression, but interestingly not with other behavioural traits or metabolic rate. Aggression is linked to interference competition, and in killifishes is often employed to secure mates, while activity and boldness are more relevant for exploiting energetic resources. Our results suggest that the trade-off between current and future reproduction plays a more prominent role in shaping mating behaviour, while behaviours related to energy acquisition may be influenced by ecological factors. This article is protected by copyright. All rights reservedPeer reviewe

The relative effects of pace of life-history and habitat characteristics on the evolution of sexual ornaments: A comparative assessment

Selection may favor greater investment into sexual ornaments when opportunities for future reproduction are limited, for example, under high adult mortality. However, predation, a key driver of mortality, typically selects against elaborate sexual ornaments. Here, we examine the evolution of sexual ornaments in killifishes, which have marked contrasts in life-history strategy among species and inhabit environments that differ in accessibility to aquatic predators. We first assessed if the size of sexual ornaments (unpaired fins) influenced swimming performance. Second, we investigated whether the evolution of larger ornamental fins is driven primarily by the pace of life-history (investment into current vs. future reproduction) or habitat type (a proxy for predation risk). We found that larger fins negatively affected swimming performance. Further, males from species inhabiting ephemeral habitats, with lower predation risk, had larger fins and greater sexual dimorphism in fin size, compared to males from more accessible permanent habitats. We show that enlarged ornamental fins, which impair locomotion, evolve more frequently in environments that are less accessible to predators, without clear associations to life-history strategy. Our results provide a rare link between the evolution of sexual ornaments, effects on locomotion performance, and natural selection on ornament size potentially through habitat differences in predation risk

Experimental Data Set

Experimental data assessing whether breeding pairs can discriminate between different, commonly encountered species of territorial intruders (intruder). We were particularly interested in testing whether pairs responded more quickly (time) to the presence of species that pose a higher level of threat to their offspring or territory, as well as assessing their subsequent rate of aggression (responses) towards the different levels of threat

Data from: Threat sensitive adjustment of aggression by males and females in a biparental cichlid

Defending offspring provides fitness benefits to parents, but is costly. To moderate costs, parents should adjust aggressive responses to the threat posed by different species entering their territory. However, few studies have experimentally tested behavioral adjustments in response to the threat posed by different types of intruders, particularly in the field, and in environments with an array of heterospecific intruders. Here, using a biparental cichlid, the poor man’s tropheus (Hypsophrys nematopus), we investigated whether males and females in the wild invest equally into offspring defense and what impact the absence of a partner might have on the quality of offspring defense provided by a solitary parent. In a separate experiment, we assessed responses of breeding pairs to three common heterospecific intruders that pose different levels of threat to the breeding pair and their brood. We found that both paired and unpaired females invested significantly more into territorial aggression than males. However, unpaired females were unable to fully compensate for the absence of their partner, with intruders left to venture closer to their offspring. Furthermore, we show that breeding pairs can readily discriminate between heterospecific intruders, with pairs responding quicker and more aggressively towards species that posed a greater potential threat. Our results demonstrate that biparental species can have extensive behavioral flexibility in their aggressive responses towards intruders, even in environments with a high frequency of territory incursion. The quality of territorial defense can nevertheless be compromised if one parent is left to defend the brood alone

Data from: Heterospecific aggression bias towards a rarer colour morph

Colour polymorphisms are a striking example of phenotypic diversity, yet the sources of selection that allow different morphs to persist within populations remain poorly understood. In particular, despite the importance of aggression in mediating social dominance, few studies have considered how heterospecific aggression might contribute to the maintenance or divergence of different colour morphs. To redress this gap, we carried out a field-based study in a Nicaraguan crater lake to investigate patterns of heterospecific aggression directed by the cichlid fish, Hypsophrys nicaraguensis, towards colour polymorphic cichlids in the genus Amphilophus. We found that H. nicaraguensis was the most frequent territorial neighbour of the colour polymorphic A. sagittae. Furthermore, when manipulating territorial intrusions using models, H. nicaraguensis were more aggressive towards the gold than dark colour morph of the sympatric Amphilophus species, including A. sagittae. Such a pattern of heterospecific aggression should be costly to the gold colour morph, potentially accounting for its lower than expected frequency and, more generally, highlighting the importance of considering heterospecific aggression in the context of morph frequencies and coexistence in the wild

Obervational Data Set

Observational data of the behaviors (aggression and chases) of breeding pairs in their natural habitat to assess sex differences in their ability to adjust aggressive responses toward intruders. This also allowed us to compare the responses of breeding pairs with naturally occurring solitary parents (i.e. individuals who are looking after the brood on their own) to determine whether the latter can compensate for the loss of their mate, with regard to the quantity (aggression_no, chase_no and aggression) and quality (aggression_initiation, chase_initiation and chase_distance) of the care they provide

Data from: Time-limited environments affect the evolution of egg - body size allometry

Initial offspring size is a fundamental component of absolute growth rate, where large offspring will reach a given adult body size faster than smaller offspring. Yet, our knowledge regarding the co-evolution between offspring and adult size is limited. In time-constrained environments, organisms need to reproduce at a high rate and reach a reproductive size quickly. In order to rapidly attain a large adult body size, we hypothesize that, in seasonal habitats, large species are bound to having a large initial size, and consequently, the evolution of egg size will be tightly matched to that of body size, compared to less time-limited systems. We tested this hypothesis in killifishes, and found a significantly steeper allometric relationship between egg size and body size in annual, compared to non-annual species. We also found higher rates of evolution of egg and body size in annual compared to non-annual species. Our results suggest that time-constrained environments impose strong selection on rapidly reaching a species-specific body size, and reproduce at a high rate, which in turn imposes constraints on the evolution of egg sizes. In combination, these distinct selection pressures result in different relationships between egg and body size among species in time-constrained versus permanent habitats