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Impact of pre-copulatory sexual cannibalism on genetic diversity and efficacy of selection

The Royal Society
Biology Letters
Authors:
Mauro Martínez Villar at Universidad de la República de Uruguay
Mauro Martínez Villar
Jesper S Bechsgaard at Aarhus University
Jesper S Bechsgaard
Trine Bilde at Aarhus University
Trine Bilde
Maria J Albo at Faculty of Sciences UdelaR//Clemente Estable Biological Research Institute
Maria J Albo
  • Faculty of Sciences UdelaR//Clemente Estable Biological Research Institute
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Abstract

Factors that increase reproductive variance among individuals act to reduce effective population size (Ne), which accelerates the loss of genetic diversity and decreases the efficacy of purifying selection. These factors include sexual cannibalism, offspring investment and mating system. Pre-copulatory sexual cannibalism, where the female consumes the male prior to mating, exacerbates this effect. We performed comparative transcriptomics in two spider species, the cannibalistic Trechaleoides biocellata and the non-cannibalistic T. keyserlingi, to generate genomic evidence to support these predictions. First, we estimated heterozygosity and found that genetic diversity is relatively lower in the cannibalistic species. Second, we calculated dN/dS ratios as a measure of purifying selection; a higher dN/dS ratio indicated relaxed purifying selection in the cannibalistic species. These results are consistent with the hypothesis that sexual cannibalism impacts operational sex ratio and demographic processes, which interact with evolutionary forces to shape the genetic structure of populations. However, other factors such as the mating system and life-history traits contribute to shaping Ne. Comparative analyses across multiple contrasting species pairs would be required to disentangle these effects. Our study highlights that extreme behaviours such as pre-copulatory cannibalism may have profound eco-evolutionary effects.
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Impact of pre-copulatory sexual
cannibalism on genetic diversity and
ecacy of selection
Mauro Martínez Villar1, Jesper Bechsgaard2, Trine Bilde2, Maria Jose Albo2,3 and
Ivanna H. Tomasco1
1Departamento de Ecología y Evolución, Facultad de Ciencias, Universidad de la República, Montevideo, 11400,
Uruguay
2Departament of Biology, Aarhus University, Aarhus 8000, Denmark
3Laboratory of Ethology, Ecology and Evolution, Clemente Estable Biological Research Institute, Montevideo,
11600, Uruguay
MMV,0000-0001-6208-2425; MJA,0000-0003-4332-7612; IHT,0000-0002-8288-8618
Factors that increase reproductive variance among individuals act to
reduce eective population size (Ne), which accelerates the loss of genetic
diversity and decreases the ecacy of purifying selection. These factors
include sexual cannibalism, ospring investment and mating system.
Pre-copulatory sexual cannibalism, where the female consumes the male
prior to mating, exacerbates this eect. We performed comparative
transcriptomics in two spider species, the cannibalistic Trechaleoides
biocellata and the non-cannibalistic T. keyserlingi, to generate genomic
evidence to support these predictions. First, we estimated heterozygosity
and found that genetic diversity is relatively lower in the cannibalistic
species. Second, we calculated dN/dS ratios as a measure of purifying
selection; a higher dN/dS ratio indicated relaxed purifying selection in
the cannibalistic species. These results are consistent with the hypothesis
that sexual cannibalism impacts operational sex ratio and demographic
processes, which interact with evolutionary forces to shape the genetic
structure of populations. However, other factors such as the mating system
and life-history traits contribute to shaping Ne. Comparative analyses
across multiple contrasting species pairs would be required to disentangle
these eects. Our study highlights that extreme behaviours such as
pre-copulatory cannibalism may have profound eco-evolutionary eects.
1. Introduction
Female sexual cannibalism is common during courtship and mating,
predominantly in predatory arthropod species [1–3]. This behaviour occurs
when a female consumes a male immediately before, during or after mating.
Sexual cannibalism impacts both individual- and population-level processes.
At the individual level, sexual cannibalism impacts the frequency and
opportunity for females to encounter mates and to exert mate choice, since
the sex ratio of mating individuals becomes female-biased and may ultimately
leave some females in the population unmated [4,5]. At the population
level, sexual cannibalism negatively impacts population growth [6], and both
the individual- and group-level eects reduce the eective population size
(Ne) of the population [7]. Overall, any process that biases the sex ratio
or increases the variance in individual reproductive success will decrease
Ne [8,9]. Pre-copulatory cannibalism has the most dramatic eects [6], as it
removes males from the pool of reproducing individuals [10,11]. Post-copu-
latory cannibalism may confer substantial fecundity benets to females but
may still have negative eects on population growth [6]. The female's mating
© 2024 The Author(s). Published by the Royal Society. All rights reserved.
Research
Cite this article: Martínez Villar M, Bechsgaard J,
Bilde T, Albo MJ, Tomasco IH. 2024 Impact of pre-
copulatory sexual cannibalism on genetic
diversity and ecacy of selection. Biol. Lett. 20:
20230505.
https://doi.org/10.1098/rsbl.2023.0505
Received: 30 May 2023
Accepted: 21 March 2024
Subject Category:
Molecular evolution
Subject Areas:
evolution, molecular biology
Keywords:
pre-copulatory cannibalism, purifying selection,
heterozygosity
Author for correspondence:
Ivanna H. Tomasco
e-mail: ivanna@fcien.edu.uy
Electronic supplementary material is available
online at https://doi.org/10.6084/
m9.gshare.c.7158530.
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