How sperm competition shapes the evolution of testes and sperm: a meta-analysis.

Published on Dec 7, 2020in Philosophical Transactions of the Royal Society B5.68
· DOI :10.1098/RSTB.2020.0064
Stefan Lüpold27
Estimated H-index: 27
(UZH: University of Zurich),
Raïssa A de Boer (Stockholm University)+ 2 AuthorsJohn L. Fitzpatrick33
Estimated H-index: 33
(Stockholm University)
Sources
Abstract
Females of many species mate with multiple males, thereby inciting competition among ejaculates from rival males for fertilization. In response to increasing sperm competition, males are predicted to enhance their investment in sperm production. This prediction is so widespread that testes size (correcting for body size) is commonly used as a proxy of sperm competition, even in the absence of any other information about a species' reproductive behaviour. By contrast, a debate about whether sperm competition selects for smaller or larger sperm has persisted for nearly three decades, with empirical studies demonstrating every possible response. Here, we synthesize nearly 40 years of sperm competition research in a meta-analytical framework to determine how the evolution of sperm number (i.e. testes size) and sperm size (i.e. sperm head, midpiece, flagellum and total length) is influenced by varying levels of sperm competition across species. Our findings support the long-held assumption that higher levels of sperm competition are associated with relatively larger testes. We also find clear evidence that sperm competition is associated with increases in all components of sperm length. We discuss these results in the context of different theoretical predictions and general patterns in the breeding biology and selective environment of sperm. This article is part of the theme issue 'Fifty years of sperm competition'.
References81
Newest
#1Shinichi Nakagawa (UNSW: University of New South Wales)H-Index: 90
#2Malgorzata Lagisz (UNSW: University of New South Wales)H-Index: 19
Last. Alistair M. Senior (USYD: University of Sydney)H-Index: 23
view all 7 authors...
: Classic" forest plots show the effect sizes from individual studies and the aggregate effect from a meta-analysis. However, in ecology and evolution meta-analyses routinely contain over 100 effect sizes, making the classic forest plot of limited use. We surveyed 102 meta-analyses in ecology and evolution, finding that only 11% use the classic forest plot. Instead, most used a "forest-like plot", showing point estimates (with 95% confidence intervals; CIs) from a series of subgroups or categori...
12 CitationsSource
#1Jonathan P. Evans (UWA: University of Western Australia)H-Index: 48
#2Rowan A. Lymbery (UWA: University of Western Australia)H-Index: 6
Broadcast spawning invertebrates offer highly tractable models for evaluating sperm competition, gamete-level mate choice and sexual conflict. By displaying the ancestral mating strategy of externa...
6 CitationsSource
#1Wen Bo Liao (CWNU: China West Normal University)H-Index: 16
#2Mao Jun Zhong (CWNU: China West Normal University)H-Index: 6
Last. Stefan Lüpold (UZH: University of Zurich)H-Index: 27
view all 3 authors...
Sperm competition is often considered the primary selective force underlying the rapid and diversifying evolution of ejaculate traits. Yet, several recent studies have drawn attention to other forms of selection with the potential of exceeding the effects of sperm competition. Since ejaculates are complex, multivariate traits, it seems plausible that different ejaculate components vary in their responses to different selective pressures. Such information, however, is generally lacking as individ...
5 CitationsSource
#1Stefan LüpoldH-Index: 27
#2Scott Pitnick (SU: Syracuse University)H-Index: 45
Sperm morphological variation has attracted considerable interest and generated a wealth of (mostly descriptive) studies over the past three centuries. Yet, apart from biophysical studies linking sperm morphology to swimming velocity, surprisingly little is known about the adaptive significance of sperm form and the selective processes underlying its tremendous diversification throughout the animal kingdom. Here, we first discuss the challenges of examining sperm morphology in an evolutionary co...
52 CitationsSource
#1Wen Bo Liao (CWNU: China West Normal University)H-Index: 16
#2Yan Huang (CWNU: China West Normal University)H-Index: 3
Last. Stefan Lüpold (UZH: University of Zurich)H-Index: 27
view all 6 authors...
: The evolution of sperm quality and quantity is shaped by various selective processes, with sperm competition generally considered the primary selective agent. Particularly in external fertilizers, however, sperm limitation through gamete dispersal can also influence gamete investments, but empirical data examining this effect are limited. Here, we studied the relative importance of sperm competition and the spawning conditions in explaining the macroevolutionary patterns of sperm size and numb...
32 CitationsSource
#1Tejinder Singh Chechi (Indian Institute of Science Education and Research, Mohali)H-Index: 1
#2Zeeshan Ali Syed (Indian Institute of Science Education and Research, Mohali)H-Index: 3
Last. Nagaraj Guru Prasad (Indian Institute of Science Education and Research, Mohali)H-Index: 18
view all 3 authors...
Sperm competition theory predicts that with increase in sperm competition, males either invest more in reproductive organ(s) and/or improve ejaculate investment. We test this idea using experimental evolution in Drosophila melanogaster. We maintained replicate populations of Drosophila melanogaster under male (M) and female (F) biased sex ratio regimes for more than a hundred generations with the result that males from the M regime evolved higher sperm competitive abilities relative to males fro...
9 CitationsSource
#1Jonathan P. Evans (UWA: University of Western Australia)H-Index: 48
#2Francisco Garcia-Gonzalez (CSIC: Spanish National Research Council)H-Index: 25
It is well known that sexual selection can target reproductive traits during successive pre- and post-mating episodes of selection. A key focus of recent studies has been to understand and quantify how these episodes of sexual selection interact to determine overall variance in reproductive success. In this article, we review empirical developments in this field but also highlight the considerable variability in patterns of pre- and post-mating sexual selection, attributable to variation in patt...
73 CitationsSource
#1Stefan Lüpold (SU: Syracuse University)H-Index: 27
#2Mollie K. Manier (SU: Syracuse University)H-Index: 20
Last. Scott Pitnick (SU: Syracuse University)H-Index: 45
view all 8 authors...
The ‘big-sperm paradox’, the observed production of few, gigantic sperm by some fruit flies (seemingly at odds with fundamental theory addressing how sexual selection works) is shown to be a result of co-evolution driven by genetic and functional relationships between sperm length, design of the female reproductive tract and features of the mating system.
68 CitationsSource
#1Geoff A. Parker (University of Liverpool)H-Index: 70
Evolutionary theory for expenditure on gonads attracted little attention until studies in the past 3–4 decades of allocation to male and female function in hermaphrodites, and of relative testes size (RTS) in animals with separate sexes. RTS appears to have varied enormously over evolutionary time, from extremely high (over 40%) in some broadcast spawners to less than 1% in some taxa with copulation and internal fertilization. Reasons for this wide evolutionary diversity in testes expenditure de...
54 CitationsSource
#1Stefan Lüpold (University of Manchester)H-Index: 27
#2John L. Fitzpatrick (University of Manchester)H-Index: 33
Postcopulatory sexual selection is widely accepted to underlie the extraordinary diversification of sperm morphology. However, why does it favour longer sperm in some taxa but shorter in others? Two recent hypotheses addressing this discrepancy offered contradictory explanations. Under the sperm dilution hypothesis, selection via sperm density in the female reproductive tract favours more but smaller sperm in large, but the reverse in small, species. Conversely, the metabolic constraint hypothes...
27 CitationsSource
Cited By21
Newest
#1Lisa Locatello (UNIPD: University of Padua)H-Index: 13
#2Oliviero Borgheresi (UNIPD: University of Padua)
Last. Maria B. Rasotto (UNIPD: University of Padua)H-Index: 25
view all 5 authors...
In many species, males can rapidly adjust their ejaculate performance in response to changing levels of sperm competition, an ability that is probably mediated by seminal fluid adaptive plasticity....
Source
#1Mrinalini (NUS: National University of Singapore)
#2Cho Yeow Koh (NUS: National University of Singapore)
Last. Nalini Puniamoorthy (NUS: National University of Singapore)H-Index: 15
view all 0 authors...
The molecular basis for the evolution of novel phenotypes is a central question in evolutionary biology. In recent years, dung beetles have emerged as models for novel trait evolution as they possess distinct precopulatory traits such as sexually dimorphic horns on their head and thorax. Here, we use functional and evolutionary genomics to investigate the origins and the evolution of postcopulatory reproductive traits in male dung beetles. Male ejaculates that underlie postcopulatory sexual sele...
Source
#1Elise Mccarthy (Macquarie University)
#2Callum S. McDiarmid (Macquarie University)H-Index: 4
Last. Simon C. Griffith (Macquarie University)H-Index: 53
view all 5 authors...
Source
#1Jun-Yan Liu (Massey University)H-Index: 6
#2Xiong Zhao He (Massey University)H-Index: 13
Last. Qiao Wang
view all 5 authors...
Theoretic and empirical studies show that social surroundings experienced by male insects during their larval or adult stage can influence their testicular investment in diverse ways. Although insect pupae do not feed and crawl, they can communicate using sex-specific and/or non-sex specific cues. Yet, it is unknown, in any insect, whether and how male pupae can fine-tune their resource allocation to sperm production and testis size in response to socio-sexual environments. We investigated this ...
Source
#1Leon GreenH-Index: 3
Last. Charlotta KvarnemoH-Index: 33
view all 8 authors...
For externally fertilising organisms in the aquatic environment, the abiotic fertilisation medium can be a strong selecting force. Among bony fishes, sperm are adapted to function in a narrow salinity range. A notable exception is the family Gobiidae, where several species reproduce across a wide salinity range. The family also contains several wide-spread invasive species. To better understand how these fishes tolerate such varying conditions, we measured sperm performance in relation to salini...
Source
#1Lena Arévalo (CSIC: Spanish National Research Council)H-Index: 4
#2Maximiliano Tourmente (CSIC: Spanish National Research Council)H-Index: 16
Last. Eduardo R. S. Roldan (CSIC: Spanish National Research Council)H-Index: 45
view all 5 authors...
Post-copulatory sexual selection is thought to influence the evolution of genes involved in reproduction. However, the detection of straightforward effects has been proven difficult due to the complexity and diversity of reproductive landscapes found in different taxa. Here, we compare the possible effect of relative testes mass as a sperm competition proxy on protamine genotype (protamine 1/protamine 2 ratio) and the link to sperm head phenotype in two rodent groups, mice, and voles. In mice, p...
Source
#1Ariel F. Kahrl (Stockholm University)H-Index: 6
#2Rhonda R. Snook (Stockholm University)H-Index: 32
Last. John L. Fitzpatrick (Stockholm University)H-Index: 33
view all 3 authors...
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 choic...
1 CitationsSource
#1G. Yu. Smirnov (RAS: Russian Academy of Sciences)H-Index: 1
#2M. V. Modorov (RAS: Russian Academy of Sciences)
Last. Yu. A. Davydova (RAS: Russian Academy of Sciences)H-Index: 5
view all 3 authors...
The levels of interspecific and intraspecific variation in morphometric parameters of spermatozoa have been studied in seven wild rodent species of the families Cricetidae and Muridae and inbred CBA mice. The study of intraspecific variability of parameters included an analysis of within-population age-related variation and variation among individuals within a population. It has been found that, as expected, animal species is the factor contributing most to variation in the test parameters, but ...
Source
Source
Sperm cells have undergone an extraordinarily divergent evolution among metazoan animals. Parker recognized that because female animals frequently mate with more than one male, sexual selection would continue after mating and impose strong selection on sperm cells to maximize fertilization success. Comparative analyses among species have revealed a general relationship between the strength of selection from sperm competition and the length of sperm cells and their constituent parts. However, com...
Source