Male ornaments can evolve through the exploitation of female perceptual biases such as those involved in responding to cues from food. This type of sensory exploitation may lead to confusion between the male signals and the cues that females use to find/recognize food. Such interference would be costly to females and may be one reason why females evolve resistance to the male ornaments. Using a group of species of viviparous fish where resistance to a sensory trap has evolved, we demonstrate that females exposed to an ornament that resembles food have a diminished foraging efficiency, that this effect is apparent when foraging on a food item with which the ornament shares visual attributes, and that not all species are equally affected by such confusion. Our results lend support to the model of ornamental evolution through chase-away sexual conflict.
Sexual reproduction brings together reproductive partners whose long-term interests often differ, raising the possibility of conflict over their reproductive investment.Males that enhance maternal investment in their offspring gain fitness benefits, even if this compromises future reproductive investment by iteroparous females. When the conflict occurs at a genomic level, it may be uncovered by crossing divergent populations, as a mismatch in the coevolved patterns of paternal manipulation and maternal resistance may generate asymmetric embryonic growth. We report such an asymmetry in reciprocal crosses between populations of the fish Girardinichthys multiradiatus.We also show that a fragment of a gene which can influence embryonic growth (Insulin-Like Growth Factor 2; igf2) exhibits a parent-of-origin methylation pattern, where the maternally inherited igf2 allele has much more 5′ cytosine methylation than the paternally inherited allele. Our findings suggest that male manipulation of maternal investment may have evolved in fish, while the parent-of-origin methylation pattern appears to be a potential candidate mechanism modulating this antagonistic coevolution process. However, disruption of other coadaptive processes cannot be ruled out, as these can lead to similar effects as conflict.
The transition from oviparity to viviparity has occurred independently over a hundred times across vertebrates, presenting a compelling case of phenotypic convergence. However, whether repeated, independent evolution of viviparity is driven by redeployment of similar genetic mechanisms and whether these leave a common genetic signature in genomic divergence remains unknown. Whilst investigations into the evolution of viviparity have demonstrated striking similarity among the genes and pathways involved across vertebrate groups, quantitative tests for genome-wide convergence provide ambivalent answers. Here, we investigate molecular convergence during independent transitions to viviparity across an order of ray-finned freshwater fish (Cyprinodontiformes). We assembled de novo and publicly-available genomes of viviparous and oviparous species to quantify molecular convergence across coding and non-coding regions. We found no evidence for an excess of molecular convergence in amino acid substitutions and rates of sequence divergence, implying independent genetic changes are associated with these transitions. However, statistical power and biological confounds (hemiplasy and introgression) could constrain our ability to detect correlated evolution. We therefore also identified candidate genes with potential signatures of molecular convergence in viviparous Cyprinodontiformes lineages. While we detected no evidence of positive or relaxed selection for these genes in branches associated with the evolution of viviparity in Cyprinodontiformes, motif-enrichment and gene ontology analyses suggest transcriptional changes associated with early morphogenesis, brain development and immunity occurred alongside the evolution of viviparity. Overall, our findings indicate that an excess of molecular convergence, at any level, is not strongly associated with independent transitions to viviparity in these fish.
Understanding the phylogeographic history of a group and identifying the factors contributing to speciation is an important challenge in evolutionary biology. Vicariance has clearly played a major role in diversification across diverse groups of organisms, but how this interacts with intrinsic biological features such as changes in reproductive system or sexual selection is less well understood. The Goodeinae are a Mexican endemic group of live-bearing fish. Here, we develop genomic resources for species within the Goodeinae and use phylogenomic approaches to characterise their evolutionary history. We sequenced, assembled and annotated the genomes of four new Goodeinae genomes, including A. toweri, the only matrotrophic live-bearing fish without a trophotaenia in the group. We produced a phylogeny of the Goodeinae and estimate timings of species divergence. We determined the extent and timing of introgression between the species to assess if this may have occurred during an early radiation, or in more recent episodes of secondary contact. We also analyse patterns in the changes of effective population size for the species and examine the time course of expansion and decline. We used branch-site models to detect genome-wide positive selection across Goodeinae, and we specifically ask if this differs in A. toweri, where reversal of placental viviparity has recently occurred. We find that Goodeinae diverged rapidly, with reductions in effective population size after each split. Contrary to expectations, we find evidence of gene flow between geographically isolated species, suggesting vicariant speciation was supplemented by limited post-speciation gene flow, potentially as a result of river piracy. Genes under positive selection in the group are likely to be associated with the switch to live-bearing. Overall, our studies suggest that both volcanism driven vicariance and changes in reproductive mode influenced radiation in the Goodeinae.
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