Evolutionary biologists have endeavoured to explain the extraordinary diversity of sperm morphology across animals for more than a century. One hypothesis to explain sperm diversity is that sperm length is shaped by the environment where fertilization takes place (that is, fertilization mode). Evolutionary transitions in fertilization modes may transform how selection acts on sperm length, probably by affecting postcopulatory mechanisms of sperm competition and the scope for cryptic female choice. Here, we address this hypothesis by generating a macro-evolutionary view of how fertilization mode (including external fertilizers, internal fertilizers and spermcasters) influences sperm length diversification among 3,233 species from 21 animal phyla. We show that sperm are shorter in species whose sperm are diluted in aquatic environments (that is, external fertilizers and spermcasters) and longer in species where sperm are directly transferred to females (that is, internal fertilizers). We also show that sperm length evolves faster and with a greater number of adaptive shifts in species where sperm operate within females (for example, spermcasters and internal fertilizers). Our results demonstrate that fertilization mode is a key driver in the evolution of sperm length across animals, and we argue that a complex combination of postcopulatory forces has shaped sperm length diversification throughout animal evolution.
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The authors thank J. Eastman, J. Uyeda, C. Cooney and C. Wheat for assistance with analyses, K. Gunnarsdóttir and H. Ogden for help proofing the dataset and supplementary references, L. Simmons and S. Lüpold for comments on an early draft of the manuscript and three reviewers for their critiques and feedback, which greatly improved this manuscript. Funding was provided by Knut and Alice Wallenberg Academy Fellowship (2016–0146) to J.L.F.
The authors declare no competing interests.
Peer review information Nature Ecology & Evolution thanks Heidi Fisher, Gustavo Burin and Matthew Gage for their contribution to the peer review of this work.
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Estimates of sperm length evolutionary optima (θ) and the rate of evolution (σ2) of sperm length for external fertilizers (blue), spermcasters (purple), and internal (red) fertilizers from OUwie models. Values are presented for all species in our dataset (a,e), Annelida (b,f), Mollusca (c,g), and Chordata (d,h). In all graphs, each point represents an estimate from an independent model run.
Extended Data Fig. 2 Magnitude, direction and the number of descendents for shifts in sperm length in each phyla.
The magnitude of each of the 108 shifts (change in theta (evolutionary optima, θ) along a branch) in sperm length plotted by phyla. The number and average magnitude of positive (+) and negative (−) shifts in each phylum is summarized under the phylum name. The direction and magnitude of each shift is indicated with an arrow, and the start (circle) and end (arrowhead) locations of the arrow show the initial and ending theta value (evolutionary optima, θ) of the shift, respectively. The vertical dashed line shows the root value of theta (θ = 4.12) estimated by bayou. The size of the circle indicates the number of descendant species (species downstream of a shift). Red symbols indicate shifts in sperm length that followed an evolutionary transition to internal fertilization (for example all species downstream of these shifts were internally fertilizing species). Blue symbols indicate shifts in sperm length all species downstream were external fertilizers. Purple symbols indicate shifts in sperm length that occurred before transitions to external fertilization and where most species were spermcasters.
The two adaptive shifts detected in the evolutionary optima (θ), and their location are presented as green (positive shift in sperm length). The size of the circle represents the magnitude of the shift (but is multiplied by 10 for visibility in this group). External fertilizers (blue), internal fertilizers (red), and spermcasters (purple) are depicted at terminal branches of the phylogeny.
The 7 adaptive shifts detected in the evolutionary optima (θ), and their location are presented as green (positive shift in sperm length) or grey (negative shift in sperm length) circles. The size of the circle represents the magnitude of the shift. External fertilizers (blue), internal fertilizers (red), and spermcasters (purple) are depicted at terminal branches of the phylogeny.
The 56 adaptive shifts detected in the evolutionary optima (θ), and their location are presented as green (positive shift in sperm length) or grey (negative shift in sperm length) circles. The size of the circle represents the magnitude of the shift. External (blue) and internal (red) fertilizers are depicted at terminal branches of the phylogeny.
Phylogenetic trees are colored with mean per-branch rates of sperm evolution (σ2BT, left) and species diversification rates (λBAMM, right) (a). Dark colors correspond to slow rates and light colors correspond to fast rates. Scatter plots showing the relationship between log-transformed tip-rates for sperm evolution (σ2BT) and species diversification rate (λBAMM) for all species (b), invertebrates (c) and vertebrates (d) (all invertebrates were combined in panel c as this was the under-sampled portion of our dataset). The trendlines for each group are plotted with 95% CI. These trendlines are based on ordinary least-squares regression, while the statistical relationships were estimated with Spearman’s rank correlation (see methods).
Nodal values of transitions between spermcasting, internal, and external fertilization summarized for 1000 SIMMAPS (used for our ancestral character reconstruction) and 100 SIMMAPS (used for OUwie models) are plotted to compare transition estimates. We found that using 100 SIMMAP trees in our analyses captures the variation seen in the 1000 SIMMAP reconstructions.
AICc estimates from OUwie models for all species in our dataset (a), Annelida (b), Mollusca (c), and Chordata (d). In all graphs, each point indicates a single estimate from each model run. The model OUMV was the best fit in all cases. OUMA and OUMVA model fits are not shown as these models did not converge properly to our data.
We used repeated resampling to validate the use of 100 SIMMAPs to estimate the evolutionary rate (θ) and evolutionary optima (σ2) of sperm length for external fertilizers (blue), spermcasters (purple), and internal fertilizers (red). We conducted 1000 iterations of resampling per each sample size of 5 to 100 estimates from our models for all species (a,e), Annelida (b,f), Mollusca (c,g), and Chordata (d,h). Generating a measure of variance in our estimate of the mean and standard deviation for both the evolutionary rate (θ) and evolutionary optima (σ2). Graphs illustrate the coefficient of variation (CV) for of these parameters for each fertilization mode.
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Kahrl, A.F., Snook, R.R. & Fitzpatrick, J.L. Fertilization mode drives sperm length evolution across the animal tree of life. Nat Ecol Evol 5, 1153–1164 (2021). https://doi.org/10.1038/s41559-021-01488-y
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