Cryptic local adaptation is pervasive across environmental and evolutionary gradients

Cryptic local adaptation—where an environmental effect masks the magnitude of the genetic contribution to a phenotype—has long been a topic of interest in ecology and evolution. Here, we systematically document the magnitude and drivers of two common forms of cryptic local adaptation—counter- and cogradient variation. Using a hierarchical Bayesian meta-analysis, we calculated the overall effect size as 1.03 for countergradient variation and 0.90 for cogradient variation. This result indicates that the genetic effect of cryptic local adaptation is approximately equal to a one standard deviation change in trait value between the most disparate populations. We also found that the abiotic and biotic covariates with the largest mean effects were temperature (2.50) and gamete size (2.78), although there was substantial variance. Our results demonstrate the pervasiveness and large effect of cryptic local adaptation in wild populations and underscores the importance of accounting for these effects in future studies.

The Legacy of Parker, Baker and Smith 1972: Gamete Competition, the Evolution of Anisogamy, and Model Robustness

The evolution of anisogamy or gamete size dimorphism is a fundamental transition in evolutionary history, and it is the origin of the female and male sexes. Although mathematical models attempting to explain this transition have been published as early as 1932, the 1972 model of Parker, Baker, and Smith is considered to be the first explanation for the evolution of anisogamy that is consistent with modern evolutionary theory. The central idea of the model is ingenious in its simplicity: selection simultaneously favours large gametes for zygote provisioning, and small gametes for numerical competition, and under certain conditions the outcome is anisogamy. In this article, I derive novel analytical solutions to a 2002 game theoretical update of the 1972 anisogamy model, and use these solutions to examine its robustness to variation in its central assumptions. Combining new results with those from earlier papers, I find that the model is quite robust to variation in its central components. This kind of robustness is crucially important in a model for an early evolutionary transition where we may only have an approximate understanding of constraints that the different parts of the model must obey.

A comparative test of the gamete dynamics theory for the evolution of anisogamy in Bryopsidales green algae

Gamete dynamics theory proposes that anisogamy arises by disruptive selection for gamete numbers versus gamete size and predicts that female/male gamete size (anisogamy ratio) increases with adult size and complexity. Evidence has been that in volvocine green algae, the anisogamy ratio correlates positively with haploid colony size. However, green algae show notable exceptions. We focus on Bryopsidales green algae. While some taxa have a diplontic life cycle in which a diploid adult (=fully grown) stage arises directly from the zygote, many taxa have a haplodiplontic life cycle in which haploid adults develop indirectly: the zygote first develops into a diploid adult (sporophyte) which later undergoes meiosis and releases zoospores, each growing into a haploid adult gametophyte. Our comparative analyses suggest that, as theory predicts: (i) male gametes are minimized, (ii) female gamete sizes vary, probably optimized by number versus survival as zygotes, and (iii) the anisogamy ratio correlates positively with diploid (but not haploid) stage complexity. However, there was no correlation between the anisogamy ratio and diploid adult stage size. Increased environmental severity (water depth) appears to drive increased diploid adult stage complexity and anisogamy ratio: gamete dynamics theory correctly predicts that anisogamy evolves with the (diploid) stage directly provisioned by the zygote.

The evolution of anisogamy does not always lead to male competition

Anisogamy has evolved in a large proportion of sexually reproducing multicellular organisms allowing the definition of the female and male sexes, producing large and small gametes, respectively. Anisogamy is the initial sexual dimorphism: it has lead the sexes to experience selection differently, which makes it a good starting point to understand the evolution of further sexual dimorphisms. For instance, it is generally accepted that anisogamy sets the stage for more intense intrasexual competition in the male sex than in the female sex. However, we argue that this idea may rely on assumptions on the conditions under which anisogamy has evolved in the first place. We consider here two widely accepted scenarios for the evolution of anisogamy: gamete competition or gamete limitation. We present a mechanistic mathematical model in which both gamete size and an intrasexual competition trait for fertilisation can coevolve in a population starting without dimorphism between its two mating types. Two different intrasexual competition traits are investigated, gamete motility and the ability of gametes to capture gametes of the opposite mating type. We show that gamete competition and gamete limitation can lead to greatly different outcomes in terms of which sex competes most for fertilisation. Our results suggest that gamete competition is most likely to lead to stronger competition in males. On the other hand, under gamete limitation, competition in form of motility can evolve in either sex while gamete capture mainly evolves in females. This study suggests that anisogamy does not per se lead to more intense male competition. The conditions under which anisogamy evolves matter, as well as the competition trait considered.

Evolution of anisogamy in the early diverging fungus, Allomyces

Gamete size dimorphism between sexes (anisogamy) is predicted to have evolved from an isogamous system in which sexes have equal-sized, monomorphic gametes. Although adaptive explanations for the evolution of anisogamy abound, we lack comparable insights into molecular changes that bring about the transition from monomorphism to dimorphism. The basal fungal clade Allomyces provides unique opportunities to investigate genomic changes that are associated with this transition in closely related species that show either isogamous or anisogamous mating systems. The anisogamous species show sexual dimorphism in gamete size, number, pigmentation and motility. We sequenced transcriptomes of five Allomyces isolates representing the two mating systems, including both male and female phenotypes in the anisogamous species. Maximum likelihood ancestral character state reconstruction performed in MESQUITE using the de-novo assembled transcriptomes indicated that anisogamy likely evolved once in Allomyces, and is a derived character as predicted in theory. We found that sexual stages of Allomyces express homologs of several genes known to be involved in sex determination in model organisms including Drosophila and humans. Furthermore, expression of CatSper homologs in male- and female-biased samples in our analysis support the hypothesis that gamete interaction in the anisogamous species of Allomyces may involve similar molecular events as the egg-sperm interaction in animals, including humans. Although the strains representing either mating system shared much of the transcriptome, supporting recent common ancestry, the analysis of rate of evolution using individual gene trees indicates high substitution rates and divergence between the strains. In summary, we find that anisogamy likely evolved once in Allomyces, using convergent mechanisms to those in other taxa.