The Darwin–Bateman paradigm recognizes competition among males for access to multiple mates as the main driver of sexual selection. Increasingly, however, females are also being found to benefit from ...multiple mating so that polyandry can generate competition among females for access to multiple males, and impose sexual selection on female traits that influence their mating success. Polyandry can reduce a male's ability to monopolize females, and thus weaken male focused sexual selection. Perhaps the most important effect of polyandry on males arises because of sperm competition and cryptic female choice. Polyandry favours increased male ejaculate expenditure that can affect sexual selection on males by reducing their potential reproductive rate. Moreover, sexual selection after mating can ameliorate or exaggerate sexual selection before mating. Currently, estimates of sexual selection intensity rely heavily on measures of male mating success, but polyandry now raises serious questions over the validity of such approaches. Future work must take into account both pre- and post-copulatory episodes of selection. A change in focus from the products of sexual selection expected in males, to less obvious traits in females, such as sensory perception, is likely to reveal a greater role of sexual selection in female evolution.
ABSTRACT
Why do some animals mate with one partner rather than many? Here, I investigate factors related to (i) spatial constraints (habitat limitation, mate availability), (ii) time constraints ...(breeding synchrony, length of breeding season), (iii) need for parental care, and (iv) genetic compatibility, to see what support can be found in different taxa regarding the importance of these factors in explaining the occurrence of monogamy, whether shown by one sex (monogyny or monandry) or by both sexes (mutual monogamy). Focusing on reproductive rather than social monogamy whenever possible, I review the empirical literature for birds, mammals and fishes, with occasional examples from other taxa. Each of these factors can explain mating patterns in some taxa, but not in all. In general, there is mixed support for how well the factors listed above predict monogamy. The factor that shows greatest support across taxa is habitat limitation. By contrast, while a need for parental care might explain monogamy in freshwater fishes and birds, there is clear evidence that this is not the case in marine fishes and mammals. Hence, reproductive monogamy does not appear to have a single overriding explanation, but is more taxon specific. Genetic compatibility is a promising avenue for future work likely to improve our understanding of monogamy and other mating patterns. I also discuss eight important consequences of reproductive monogamy: (i) parentage, (ii) parental care, (iii) eusociality and altruism, (iv) infanticide, (v) effective population size, (vi) mate choice before mating, (vii) sexual selection, and (viii) sexual conflict. Of these, eusociality and infanticide have been subject to debate, briefly summarised herein. A common expectation is that monogamy leads to little sexual conflict and no or little sexual selection. However, as reviewed here, sexual selection can be substantial under mutual monogamy, and both sexes can be subject to such selection. Under long‐term mutual monogamy, mate quality is obviously more important than mate numbers, which in turn affects the need for pre‐mating mate choice. Overall, I conclude that, despite much research on genetic mating patterns, reproductive monogamy is still surprisingly poorly understood and further experimental and comparative work is needed. This review identifies several areas in need of more data and also proposes new hypotheses to test.
Invasive species may quickly colonize novel environments, which could be attributed to both phenotypic plasticity and an ability to locally adapt. Reproductive traits are expected to be under strong ...selection when the new environment limits reproductive success of the invading species. This may be especially important for external fertilizers, which release sperm and eggs into the new environment. Despite adult tolerance to high salinity, the invasive fish Neogobius melanostomus (round goby) is absent from fully marine regions of the Baltic Sea, raising the possibility that its distribution is limited by tolerance during earlier life stages. Here, we investigate the hypothesis that the spread of N. melanostomus is limited by sperm function in novel salinities. We sampled sperm from two invasion fronts with higher and lower salinities in the Baltic Sea and tested them across a range of salinity levels. We found that sperm velocity and percentage of motile sperm declined in salinity levels higher and lower than those currently experienced by the Baltic Sea populations, with different performance curves for the two fronts. Sperm velocity also peaked closer to the home salinity conditions in each respective invasion front, with older localities showing an increased fit to local conditions. By calculating how the sperm velocity has changed over generations, we show this phenotypic shift to be in the range of other fish species under strong selection, indicating ongoing local adaptation or epigenetic acclimation to their novel environment. These results show that while immigrant reproductive dysfunction appears to at least partly limit the distribution of invasive N. melanostomus in the Baltic Sea, local adaptation to novel environments could enable future spread beyond their current boundaries.
In species where females compete for mates, the male often provides the female with resources in addition to gametes. A recently suggested definition of sexual selection proposed that if females only ...benefit from additional resources that come with each mating and not additional gametes, female intrasexual competition for mating opportunities would result in natural selection rather than sexual selection. The nuptial gift-giving bushcricket
has dynamic sex roles and has been a textbook example of sexual selection acting on females via mating competition. We investigated whether females of this species gain fitness benefits from nuptial gifts, additional ejaculates or both by controlling the number of matings and whether the female was allowed to consume the nutritious gift (spermatophylax) at mating. We found that egg production per day of life increased with the number of additional matings, both with and without spermatophylax consumption, but consuming the spermatophylax had an additional positive effect on the number of eggs. These effects were particularly strong in females with shorter lifespans. We discuss how the recently suggested definition of sexual selection applies to nuptial-feeding insects and conclude that both natural and sexual selections influence mating competition in
females.
Anthropogenic underwater noise is a global pollutant of increasing concern but its impact on reproduction in fish is largely unknown. Hence, a better understanding of its consequences for this ...important link to fitness is crucial. Working in aquaria, we experimentally tested the impact of broadband noise exposure (added either continuously or intermittently), compared to a control, on the behaviour and reproductive success of the common goby (Pomatoschistus microps), a vocal fish with exclusive paternal care. Compared to the intermittent noise and control treatments, the continuous noise treatment increased latency to female nest inspection and spawning and decreased spawning probability. In contrast, many other female and male pre-spawning behaviours, and female ventilation rate (proxies for stress levels) did not differ among treatments. Therefore, it is likely that female spawning decisions were delayed by a reduced ability to assess male acoustic signals, rather than due to stress per se and that the silent periods in the intermittent noise treatment provided a respite where the females could assess the males. Taken together, we show that noise (of similar frequency range as anthropogenic boat noise) negatively affects reproductive success, particularly under a continuous noise exposure.
Trade-offs between brood size and offspring size, offspring survival, parental condition or parental survival are classic assumptions in life history biology. A reduction in brood size may lessen ...these costs of care, but offspring mortality can also result in an energetic gain, if parents are able to utilize the nutrients from the demised young. Males of the broad-nosed pipefish (Syngnathus typhle) care for the offspring by brooding embryos in a brood pouch. Brooding males can absorb nutrients that emanate from embryos, and there is often a reduction in offspring number over the brooding period. In this study, using two experimentally determined brood sizes (partially and fully filled brood pouches), we found that full broods resulted in larger number of developing offspring, despite significantly higher absolute and relative embryo mortality, compared to partial broods. Male survival was also affected by brood size, with males caring for full broods having poorer survival, an effect that together with the reduced embryo survival was found to negate the benefit of large broods. We found that embryo mortality was lower when the brooding males were in good initial condition, that embryos in broods with low embryo mortality weighed more, and surprisingly, that males in higher initial condition had embryos of lower weight. Brood size, however, did not affect embryo weight. Male final condition, but not initial condition, correlated with higher male survival. Taken together, our results show costs and benefits of caring for large brood sizes, where the numerical benefits come with costs in terms of both embryo survival and survival of the brooding father, effects that are often mediated via male condition.
Sperm performance is often tightly linked to male reproductive success. In many demersal gobiid fishes, the male attaches sperm embedded in a mucus produced by sperm-duct glands to the nest substrate ...before spawning takes place. Sperm are activated as the mucus and embedded gland content dissolve into the water. To test the importance of gland content on sperm function in Pomatoschistus minutus, a marine fish with external fertilization, we used a paired experimental design, with spermatozoa tested with and without sperm-duct gland content mixed into seawater. We measured sperm velocity, percentage of motile sperm and sperm viability over time. Sperm were found to swim 7.3% faster when gland content was mixed in the seawater. Percentage motile sperm was unaffected by the gland content. Sperm viability in seawater exceeded 24 h, but was unaffected by the gland content. An increase in sperm velocity of similar magnitude as found here has been shown by others to increase fertilization success. Since velocity-boosting properties of sperm-duct gland content have now been found in three distantly related goby species, this trait appears to be conserved across the Gobiidae family and may aid in reproduction across a range of species and environments. This article has an associated First Person interview with the first author of the paper.
Studies of colonization of new habitats that appear from rapidly changing environments are interesting and highly relevant to our understanding of divergence and speciation. Here, we analyse ...phenotypic and genetic variation involved in the successful establishment of a marine fish (sand goby, Pomatoschistus minutus) over a steep salinity drop from 35 PSU in the North Sea (NE Atlantic) to two PSU in the inner parts of the post‐glacial Baltic Sea. We first show that populations are adapted to local salinity in a key reproductive trait, the proportion of motile sperm. Thereafter, we show that genome variation at 22,190 single nucleotide polymorphisms (SNPs) shows strong differentiation among populations along the gradient. Sequences containing outlier SNPs and transcriptome sequences, mapped to a draft genome, reveal associations with genes with relevant functions for adaptation in this environment but without overall evidence of functional enrichment. The many contigs involved suggest polygenic differentiation. We trace the origin of this differentiation using demographic modelling and find the most likely scenario is that at least part of the genetic differentiation is older than the Baltic Sea and is a result of isolation of two lineages prior to the current contact over the North Sea–Baltic Sea transition zone.
Using a combined experimental, genomic and demographic inference approach, we study the establishment of sand goby over a steep salinity gradient from the North Sea to the Baltic Sea. Sperm motility and outlier SNPs support local adaptation along the gradient, whereas demographic inference suggests that this adaptation involved ancient genetic variants having evolved either in glacial refugia or during ancient expansion wave before the Baltic Sea colonization.
During male–male competition, evolution can favor alternative reproductive tactics. This often results in a dominant morph that holds a resource, such as a nest for egg laying, which competes with a ...smaller sneaker morph that reproduces by stealing fertilizations. The salinity environment can influence male growth rates, for example, via osmoregulatory costs, which in turn may influence the use of sneaker tactics for small males competing for mating opportunities. Salinity can also affect sperm directly; however, little is known of how salinity influences sneaker tactics through sperm performance. We sampled males of the invasive round goby (Neogobius melanostomus) from two environments, a freshwater river and a brackish estuary. This fish has two male morphs: nest‐holding dark males and non‐nest‐holding light males. We examined the role of water salinity of 0, 8, and 16 on sperm performance and found that for estuarine males, a salinity of 0 reduced sperm velocity compared to a salinity of 8 and 16. Riverine males had low velocity in all salinities. Sperm viability also decreased by over 30% in 0 salinity, compared to 8 and 16, for fish from both environments. Gobies produce ejaculate contents in specialized glands that could in theory shield sperm in an adverse environment. However, gland contents did not improve sperm performance in our tests. Body mass and age estimates indicate that riverine males invested more in somatic growth compared to estuarine males. Estuarine light morph males had a high enough gonadosomatic index to indicate sneaker tactics. We propose that when sperm performance is low, such as for the riverine males, sneaker tactics are ineffective and will be selected against or phenotypically suppressed. Instead, we interpret the increased investment in somatic growth found in riverine males as a life‐history decision that is advantageous when defending a nest in the next reproductive season.
For a male fish too small to defend mating resources such as a female or her eggs, siring offspring can be achieved by sneaking into another male's nest and ejaculating there. In the invasive round goby, this alternative tactic requires sperm to function long enough to fertilize the eggs. This fish has spread into a range of salinities, but for some populations, fresh water decreases sperm velocity and lifespan, and severely limits the use of these alternative reproductive tactics to the point where they may disappear from use.
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