Propagule size and sex ratio influence colonisation dynamics after introduction of a non-native lizard.

The composition of founding populations plays an important role in colonisation dynamics and can influence population growth during early stages of biological invasion. Specifically, founding populations with small propagules (i.e. low number of founders) are vulnerable to the Allee effect and have reduced likelihood of establishment compared to those with large propagules. The founding sex ratio can also impact establishment via its influence on mating success and offspring production. Our goal was to test the effects of propagule size and sex ratio on offspring production and annual population growth following introductions of a non-native lizard species (Anolis sagrei). We manipulated propagule composition on nine small islands, then examined offspring production, population growth and survival rate of founders and their descendants encompassing three generations. By the third reproductive season, per capita offspring production was higher on islands seeded with a relatively large propagule size, but population growth was not associated with propagule size. Propagule sex ratio did not affect offspring production, but populations with a female-biased propagule had positive growth, whereas those with a male-biased propagule had negative growth in the first year. Populations were not affected by propagule sex ratio in subsequent years, possibly due to rapid shifts towards balanced (or slightly female biased) population sex ratios. Overall, we show that different components of population fitness have different responses to propagule size and sex ratio in ways that could affect early stages of biological invasion. Despite these effects, the short life span and high fecundity of A. sagrei likely helped small populations to overcome Allee effects and enabled all populations to successfully establish. Our rare experimental manipulation of propagule size and sex ratio can inform predictions of colonisation dynamics in response to different compositions of founding populations, which is critical in the context of population ecology and invasion dynamics.

Rapid evolution of testis size relative to sperm morphology suggests that post-copulatory selection targets sperm number in Anolis lizards.

Post-copulatory sexual selection is thought to be responsible for much of the extraordinary diversity in sperm morphology across metazoans. However, the extent to which post-copulatory selection targets sperm morphology versus sperm production is generally unknown. To address this issue, we simultaneously characterized the evolution of sperm morphology (length of the sperm head, midpiece and flagellum) and testis size (a proxy for sperm production) across 26 species of Anolis lizards, a group in which sperm competition is likely. We found that the length of the sperm midpiece has evolved 2-3 times faster than that of the sperm head or flagellum, suggesting that midpiece size may be the most important aspect of sperm morphology with respect to post-copulatory sexual selection. However, testis size has evolved faster than any aspect of sperm morphology or body size, supporting the hypothesis that post-copulatory sexual selection acts more strongly upon sperm production than upon sperm morphology. Likewise, evolutionary increases in testis size, which typically indicate increased sperm competition, are not associated with predictable changes in sperm morphology, suggesting that any effects of post-copulatory selection on sperm morphology are either weak or variable in direction across anoles. Collectively, our results suggest that sperm production is the primary target of post-copulatory sexual selection in this lineage.

Sperm morphology and count vary with fine-scale changes in local density in a wild lizard population.

Given that sperm production can be costly, theory predicts that males should optimally adjust the quantity and/or quality of their sperm in response to their social environment to maximize their paternity success. Although experiments demonstrate that males can alter their ejaculates in response to manipulations of the social environment and studies show that ejaculate traits covary with social environment across populations, it is unknown whether individual variation in sperm traits corresponds to natural variation found within wild populations. Using an island population of brown anole lizards (Anolis sagrei), we tested the prediction that sperm traits (sperm count, sperm morphology, sperm velocity) respond to natural variation in the risk of sperm competition, as inferred from the local density and operational sex ratio (OSR) of conspecifics. We found that males living in high-density areas of the island produced relatively larger sperm midpieces, smaller sperm heads, and lower sperm counts. Sperm traits were unrelated to OSR after accounting for the covariance between OSR and density. Our findings broaden the implications of sperm competition theory to intrapopulation social environment variation by showing that sperm count and sperm morphology vary with fine-scale differences in density within a single wild population.

Does adaptive radiation of a host lineage promote ecological diversity of its bacterial communities? A test using gut microbiota of Anolis lizards.

Adaptive radiations provide unique opportunities to test whether and how recent ecological and evolutionary diversification of host species structures the composition of entire bacterial communities. We used 16S rRNA gene sequencing of faecal samples to test for differences in the gut microbiota of six species of Puerto Rican Anolis lizards characterized by the evolution of distinct 'ecomorphs' related to differences in habitat use. We found substantial variation in the composition of the microbiota within each species and ecomorph (trunk-crown, trunk-ground, grass-bush), but no differences in bacterial alpha diversity among species or ecomorphs. Beta diversity analyses revealed subtle but significant differences in bacterial composition related to host phylogeny and species, but these differences were not consistently associated with Anolis ecomorph. Comparison of a trunk-ground species from this clade (A. cristatellus) with a distantly related member of the same ecomorph class (A. sagrei) where the two species have been introduced and are now sympatric in Florida revealed pronounced differences in the alpha diversity and beta diversity of their microbiota despite their ecological similarity. Comparisons of these populations with allopatric conspecifics also revealed geographic differences in bacterial alpha diversity and beta diversity within each species. Finally, we observed high intraindividual variation over time and strong effects of a simplified laboratory diet on the microbiota of A. sagrei. Collectively, our results indicate that bacterial communities are only weakly shaped by the diversification of their lizard hosts due to the strikingly high levels of bacterial diversity and variation observed within Anolis species.

SpermTree, a species-level database of sperm morphology spanning the animal tree of life.

Sperm are the most morphologically variable cell type known, despite performing the same functional role of fertilizing eggs across all sexually reproducing species. Sperm morphology commonly varies among individuals, populations, closely related species, and across animal phyla. Sperm morphology has long been used as a tool for placing species in a phylogenetic context and a range of selective forces are hypothesized to influence sperm evolution and diversification. However, we currently lack robust examinations of macroevolutionary (i.e. across phyla) patterns of sperm evolution, due largely to the challenges of comparing sperm morphological data across the animal tree of life. Here we describe the SpermTree database, which currently represents 5,675 morphological descriptions of sperm morphology from 4,705 unique species from 27 animal phyla. This dataset includes measurements of sperm head, midpiece, flagellum and total length, the latter of which spans four orders of magnitude. All entries in the dataset are matched to currently accepted scientific names in taxonomic databases, facilitating the use of these data in analyses examining sperm evolution in animals.

Fertilization mode differentially impacts the evolution of vertebrate sperm components.

Environmental change frequently drives morphological diversification, including at the cellular level. Transitions in the environment where fertilization occurs (i.e., fertilization mode) are hypothesized to be a driver of the extreme diversity in sperm morphology observed in animals. Yet how fertilization mode impacts the evolution of sperm components-head, midpiece, and flagellum-each with different functional roles that must act as an integrated unit remains unclear. Here, we test this hypothesis by examining the evolution of sperm component lengths across 1103 species of vertebrates varying in fertilization mode (external vs. internal fertilization). Sperm component length is explained in part by fertilization mode across vertebrates, but how fertilization mode influences sperm evolution varies among sperm components and vertebrate clades. We also identify evolutionary responses not influenced by fertilization mode: midpieces evolve rapidly in both external and internal fertilizers. Fertilization mode thus influences vertebrate sperm evolution through complex component- and clade-specific evolutionary responses.

Resource-dependent investment in male sexual traits in a viviparous fish.

Exaggerated and conspicuous sexually selected traits are often costly to produce and maintain. Costly traits are expected to show resource-dependent expression, since limited resources prevent animals from investing maximally in multiple traits simultaneously. However, there may be critical periods during an individual's life where the expression of traits is altered if resources are limited. Moreover, costly sexual traits may arise from sexual selection acting both before (pre-copulatory) and after mating (post-copulatory). Gaining a robust understanding of resource-dependent trait expression therefore requires an approach that examines both episodes of sexual selection after resource limitation during different times in an individual's life. Yet few studies have taken such an approach. Here, we examine how resource restriction influences a set of pre- and post-copulatory traits in male pygmy halfbeaks (Dermogenys collettei), which invest in sexual ornaments and routinely engage in male-male contests and sperm competition. Critically, we examined responses in males when resources were restricted during development and after reaching sexual maturity. Both pre- and post-copulatory traits are resource-dependent in male halfbeaks. Body size, beak size, courtship behavior, and testes size were reduced by diet restriction, while, unexpectedly, the restricted-diet group had a larger area of red color on the beak and fins after diet treatment. These patterns were generally consistent when resources were restricted during development and after reaching sexual maturity. The study reinforces the role of resource acquisition in maintaining variation among sexual traits.

Fertilization mode drives sperm length evolution across the animal tree of life.

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.

Corrigendum to: Male-male behavioral interactions drive social-dominance mediated differences in ejaculate traits.

[This corrects the article DOI: 10.1093/beheco/araa118.].

Selection on Sperm Count, but Not on Sperm Morphology or Velocity, in a Wild Population of Anolis Lizards.

Sperm competition is a widespread phenomenon that shapes male reproductive success. Ejaculates present many potential targets for postcopulatory selection (e.g., sperm morphology, count, and velocity), which are often highly correlated and potentially subject to complex multivariate selection. Although multivariate selection on ejaculate traits has been observed in laboratory experiments, it is unclear whether selection is similarly complex in wild populations, where individuals mate frequently over longer periods of time. We measured univariate and multivariate selection on sperm morphology, sperm count, and sperm velocity in a wild population of brown anole lizards (Anolis sagrei). We conducted a mark-recapture study with genetic parentage assignment to estimate individual reproductive success. We found significant negative directional selection and negative quadratic selection on sperm count, but we did not detect directional or quadratic selection on any other sperm traits, nor did we detect correlational selection on any trait combinations. Our results may reflect pressure on males to produce many small ejaculates and mate frequently over a six-month reproductive season. This study is the first to measure multivariate selection on sperm traits in a wild population and provides an interesting contrast to experimental studies of external fertilizers, which have found complex multivariate selection on sperm phenotypes.

Male-male behavioral interactions drive social-dominance-mediated differences in ejaculate traits.

Higher social status is expected to result in fitness benefits as it secures access to potential mates. In promiscuous species, male reproductive success is also determined by an individual's ability to compete for fertilization after mating by producing high-quality ejaculates. However, the complex relationship between a male's investment in social status and ejaculates remains unclear. Here, we examine how male social status influences ejaculate quality under a range of social contexts in the pygmy halfbeak Dermogenys collettei, a small, group-living, internally fertilizing freshwater fish. We show that male social status influences ejaculate traits, both in the presence and absence of females. Dominant males produced faster swimming and more viable sperm, two key determinants of ejaculate quality, but only under conditions with frequent male-male behavioral interactions. When male-male interactions were experimentally reduced through the addition of a refuge, differences in ejaculate traits of dominant and subordinate males disappeared. Furthermore, dominant males were in a better condition, growing faster, and possessing larger livers, highlighting a possible condition dependence of competitive traits. Contrary to expectations, female presence or absence did not affect sperm swimming speed or testes mass. Together, these results suggest a positive relationship between social status and ejaculate quality in halfbeaks and highlight that the strength of behavioral interactions between males is a key driver of social-status-dependent differences in ejaculate traits.

Sperm competition in squamate reptiles.

Multiple paternity is ubiquitous within the polyphyletic group called 'reptiles', especially within the lizards and snakes. Therefore, the probability of sperm competition occurring, and being intense, is high. Squamates exhibit a diversity of tactics to ensure fertilization success in the face of sperm competition. The duration of female sperm storage, which can be many months and even years in some species, remains an enigma. Here, we emphasize some mechanisms that might affect patterns of paternity, the source and function of ejaculates and features of the female reproductive tract that may aid in long-term sperm storage. In doing so, we present a new analysis of the relationship between sperm size, the strength of sperm competition and the duration of female sperm storage. Lizards and snakes are a diverse group that has provided many excellent models for the study of an array of life-history strategies. However, when it comes to postcopulatory sexual selection, there is much left to discover. This article is part of the theme issue 'Fifty years of sperm competition'.

Contrasting female mate preferences for red coloration in a fish.

Understanding how animals select their mates requires knowing the factors that shape mate preferences. Recent theoretical and empirical considerations suggest that female mating status can influence the degree to which a female engages in mate choice, with virgin females predicted to be less choosy than mated females. In this study, we investigated mate choice in both virgin and mated females in the pygmy halfbeak Dermogenys collettei. Halfbeaks are small, live-bearing, internally fertilizing freshwater fish that live in mixed-sex groups where females have ample opportunity to engage in mate choice. Using a dichotomous choice assay, we quantified and contrasted in virgin and mated females mate preferences for differences in male body size, beak size, and area of yellow and red coloration. We also examined how mating status influenced the amount of time a female associated with the first male encountered and the relative amount of time a female associated with each male. We demonstrate that mate preferences of female halfbeaks are driven primarily by the size of red coloration present on males. Females showed contrasting preferences based on mating status, with virgin females preferentially associating with drab males whereas mated females preferentially associate with males possessing large areas of red. Contrary to expectations, female mating status did not influence how females associate with the first males encountered or how females biased their association time among males. Although the precise drivers of these effects need further studying, our finding highlights a possible explanation for how variation in male ornamentation can be maintained.

Male mate choice for large gravid spots in a livebearing fish.

Male mate choice occurs in a wide range of species, and males can increase their reproductive success by distinguishing between females based on their fecundity (e.g., large body size) or their expected sperm competition risk (e.g., virgins). However, patterns of male mate choice could be mitigated by variation in female physiological receptivity, as males can benefit by directing their mating efforts toward females that are at a point in their reproductive cycle when fertilization probability is highest. Here, we perform three experiments to assess whether male mate choice is influenced by cues of female physiological receptivity, fecundity, or sperm competition risk in the pygmy halfbeak (Dermogenys collettei), a small livebearing fish. Female halfbeaks possess a "gravid spot"-an orange abdominal marking that is caused by pigmentation of the females' skin and variation in embryo development and pigmentation during pregnancy. We show that gravid spot size increases toward parturition and is largest right before giving birth, independent of abdominal width or body size. Males consistently chose females with large gravid spots over females with small gravid spots. In contrast, males did not prefer larger females over smaller females or virgin females over mated females. As female halfbeaks store sperm prior to fertilizations, we suggest that males use the size of the gravid spot as a cue to direct their mating efforts to those females where the chance of fertilization is highest.

Correlated evolution between targets of pre- and postcopulatory sexual selection across squamate reptiles.

Sexual selection reflects the joint contributions of precopulatory selection, which arises from variance in mating success, and postcopulatory selection, which arises from variance in fertilization success. The relative importance of each episode of selection is variable among species, and comparative evidence suggests that traits targeted by precopulatory selection often covary in expression with those targeted by postcopulatory selection when assessed across species, although the strength and direction of this association varies considerably among taxa. We tested for correlated evolution between targets of pre- and postcopulatory selection using data on sexual size dimorphism (SSD) and testis size from 151 species of squamate reptiles (120 lizards, 31 snakes). In squamates, male-male competition for mating opportunities often favors large body size, such that the degree of male-biased SSD is associated with the intensity of precopulatory selection. Likewise, competition for fertilization often favors increased sperm production, such that testis size (relative to body size) is associated with the intensity of postcopulatory selection. Using both conventional and phylogenetically based analyses, we show that testis size consistently decreases as the degree of male-biased SSD increases across lizards and snakes. This evolutionary pattern suggests that strong precopulatory selection may often constrain the opportunity for postcopulatory selection and that the relative importance of each selective episode may determine the optimal resolution of energy allocation trade-offs between traits subject to each form of sexual selection.