Cryptic Diversity and Sexual Selection

Recent advances in molecular and genetic techniques have revealed tremendous hidden genetic diversity in plants and animals. Crustaceans are no exception and, in fact, present one of the highest levels of cryptic diversity among the metazoans. Beyond the importance of such discovery and its multiple implications for taxonomy and ecology, it is now timely to investigate the potential causes of cryptic diversity. This chapter reviews the theoretical and experimental literature, seeking evidences for a relationship between sexual selection and cryptic diversity in crustaceans. It proposes three scenarios for the role of sexual selection on the origin and maintenance of pre-mating isolation and genetic divergence among crustacean populations, and suggests ways to discriminate among them experimentally or using existing data. Assuming that taxonomic identification is largely based on differences in sexually selected morphological traits, it also reviews evidence for a cryptic action of sexual selection on crustacean phenotypes. Specifically, if sexual selection acts primarily on chemical, visual, or behavioral traits, it is likely that allopatric crustacean populations remain morphologically similar even when they are reproductively isolated. This review shows that the strength of sexual selection likely differs among allopatric populations but does not seem to consistently induce pre-mating isolation (e.g. as in copepods and amphipods). Research is now needed to try to identify general patterns and determine the role of sexual selection on pre-mating isolation after secondary contact between populations, through reinforcement and reproductive character displacement.

Multiple Matings and Sperm Competition

In polyandrous mating systems, females mate multiple times and males have evolved adaptations for sperm competition which increase the number and fitness of their offspring. Mate guarding is a widespread monopolization strategy in groups where female receptivity is temporally restricted and often associated with the molt. Precopulatory guarding occurs in branchipods, copepods, peracarids and decapods. Postcopulatory guarding is notable in numerous brachyurans with males protecting females until her exoskeleton has hardened. During copulation, male success in fertilization depends on an effective sperm transfer mechanism, the precise placement of ejaculates closest to where female gametes are fertilized. Male copulatory systems are highly diverse and strongly adapted to these tasks, especially the structures that interact with the female genital ducts. The elaborate tips of brachyuran gonopods are supposed to act in the displacement, possibly even in the removal of rival sperm masses; however, sperm removal is only evident in crayfish: males eat spermatophores previously deposited by other males. During copulation of several crustacean groups, males transfer secretions that harden and form a sealant. These sperm plugs, plaques and gel layers may protect their own sperm, prevent remating or seal off rival sperm from the site of fertilization. Several groups of isopods and decapods have internal insemination, elaborate sperm storage organs and some exhibit internal fertilization. The intensity of sperm competition increases with the latency between the processes of insemination and fertilization. This chapter gives on overview on mate guarding, male sealants and the anatomical adaptations to sperm competition in crustaceans. We also briefly discuss the consequences of multiple matings for the genetic diversity of broods, i.e., single vs. multiple paternities. There is still a lack of data for many crustacean groups. Moreover, it is often hard to assess how successful a male strategy to ensure paternity actually is as many studies focus on either the behavioral, anatomical, or molecular aspects, while comprehensive multi-level studies on crustacean sperm competition are virtually absent from the literature.

Alternative Reproductive Tactics

Alternative reproductive tactics (ARTs) describe variation among individuals of a single sex in the tactics used to obtain mating opportunities. In crustaceans, ARTs have been observed in multiple taxa and take a variety of forms. ARTs are most commonly observed in males and are generally associated with intense competition among males to monopolize access to breeding females. ARTs frequently involve a guard tactic that competes with other males to monopolize access to females, while a second usurper tactic foregos competition with other males and instead obtains mating opportunities through sneaking behavior. Guard and usurper tactics may be expressed conditionally based on a male’s ability to guard a female (e.g. his body size, the abundance of competitors), or may be expressed as discrete phenotypes that can also include morphological differentiation. For example, in Jassa amphipods the guard tactic is associated with large body size and an enlarged “thumb” on the claw that is used in aggressive interactions with other males, while the usurper tactic is associated with small body size and a reduced thumb. The usurper tactic can take two forms in a marine isopod: small males (gamma) use sneaking behavior to avoid competition with large males (alpha), whereas intermediate-sized males (beta) use female mimicry to avoid competition. Overall, ARTs are well-represented in crustaceans, with many opportunities for continued study to better characterize these unique adaptations.

Hermaphroditism and Gonochorism

This chapter compares two sexual systems: hermaphroditism (each individual can produce gametes of either sex) and gonochorism (each individual produces gametes of only one of the two distinct sexes) in crustaceans. These two main sexual systems contain a variety of alternative modes of reproduction, which are of great interest from applied and theoretical perspectives. The chapter focuses on the description, prevalence, analysis, and interpretation of these sexual systems, centering on their evolutionary transitions. The ecological correlates of each reproductive system are also explored. In particular, the prevalence of “unusual” (non-gonochoristic) reproductive strategies has been identified under low population densities and in unpredictable/unstable environments, often linked to specific habitats or lifestyles (such as parasitism) and in colonizing species. Finally, population-level consequences of some sexual systems are considered, especially in terms of sex ratios. The chapter aims to provide a broad and extensive overview of the evolution, adaptation, ecological constraints, and implications of the various reproductive modes in this extraordinarily successful group of organisms.

Environmental Influences on Crustacean Sex Determination and Reproduction: Environmental Sex Determination, Parasitism, and Pollution

This chapter reviews the influences of environmental factors on sex determination, sex ratios, and reproductive behavior in the Crustacea, focusing in particular on amphipod and isopod examples. A range of abiotic and biotic environmental factors influence reproduction in Crustacea, including temperature, day length, pollutants, and parasites. Individual crustaceans may benefit from these environmental influences, but in other cases, reproductive biology responses to biotic and abiotic environments may be detrimental to individual fitness. Environmental Sex Determination (ESD) falls into the former category. ESD is an adaptive mechanism of sex determination that is rare, but has evolved in diverse taxa. Evidence from gammarid amphipods is used to explore the evolution of ESD in response to a patchy environment. While ESD is an adaptive mechanism of sex determination, the impact of other environmental factors can be very costly. Parasitic castrators can lead to a reduction or total cessation of reproduction in crustacean hosts, driving population declines. In contrast, parasitic feminizers convert male hosts into females, enhancing maternal parasite transmission but also leading to sex ratio distortion in the host population. The chapter discusses parasite-host coevolutionary conflict and reviews evidence that selection on the host in response to parasitic sex ratio distortion has led to altered mate choice in amphipods, and to the evolution of a novel system of sex determination in isopods. Human-induced environmental influences can also be seen in Crustacea, and the chapter discusses how parasites, ESD, and endocrine-disrupting chemicals can each affect sex determination and lead to abnormal intersex phenotypes. It ends by highlighting areas for future research on the diverse world of crustacean reproduction.

Detecting Cryptic Female Choice in Decapod Crustaceans

Decapod Crustacea (shrimps, lobsters, and crabs) employ a range of different reproductive mechanisms that affect paternity, but does it include cryptic female choice (CFC)? This chapter focuses on events surrounding the fertilization of an egg by a sperm and the opportunities where cryptic fertilization bias might occur. It presents a new model of decapod fertilization, defined in terms of space and time to fertilization. Females have several ways to store sperm and influence fertilization outcomes, which should be affected by (1) their growth pattern (indeterminate or determinate), (2) the link between molting and mating (soft-shell or hard-shell mating), (3) fertilization latency, and (4) how sperm are protected (no protection or storage is separate from the oviduct, or storage in a seminal receptacle is linked to the oviduct). Paternity data available for 26 decapods show that in 85% of species, females carry broods with multiple paternity and 15% have broods with single paternity. Therefore many (if not most) females mate with several males and so they certainly could make a choice. However, whether this pattern is due to CFC or merely reflects mating history is a matter of debate. At present, there are no unequivocal data that demonstrate CFC: outcomes caused by male mate guarding and sperm competition cannot be distinguished from female choice. The challenge is to understand what females might be choosing and how to detect that choice. Detecting CFC in field data is difficult, if not impossible, because both single and multiple paternities could be favored.

Rhythms and Reproduction

Reproductive rhythms can be found in numerous crustacean species. This chapter reviews the temporal scales of rhythms and how these rhythms are entrained and maintained by external cues and endogenous clocks. The occurrence and synchrony of rhythms vary along latitudinal and depth gradients, which may depend on the availability of zeitgebers (e.g., temperature and photoperiod), changing selective pressures such as predation risk, and variability in larval development rates that affect the timing and synchrony of reproductive rhythms. Commonly observed rhythms are reproductive migrations and synchronized larval release, which are often timed to reduce predation risk for newly hatched larvae. In crustaceans, reproductive rhythms rarely evolve under pure density-dependent selection for synchrony. Pure density dependence is common in marine broadcast-spawning invertebrates like corals, which rely on accumulation of gametes in time and space to ensure fertilization. Instead, (density-independent) selection for synchrony with environmental cycles that track changes in factors affecting fitness such as energy expenditure, predation risk, or food availability seems to be the rule, although some exceptions may exist. In contrast to natural selection, the possible contribution of sexual selection on reproductive rhythms has rarely been considered. Selection for enhanced mating possibilities should favor reproductive synchrony, but deviations from synchrony will affect the operational sex ratio and influence sexual selection. Finally, the chapter discusses the possibility of sexual conflict over reproductive timing between males and females and explores circumstances under which synchronous reproductive rhythms might be abandoned.

An Evolutionary Ecological Approach to Sex Allocation and Sex Determination in Crustaceans

This chapter reviews sex determination and sex allocation strategies among crustaceans with different sexual systems (gonochorism, sequential and simultaneous hermaphroditism, and androdioecy), from the perspective of evolutionary ecology. The discussion includes genetic, environmental, and cytoplasmic sex determination in free-living and parasitic crustaceans, timing and frequency of sex change especially in partial protandry, the effects of mating group size on resource allocation by simultaneous hermaphrodites, and sex ratio and determination in androdioecious crustaceans. The fascinating diversity of crustacean reproduction stimulated theoretical biologists to construct models to explain them, and empirical biologists attempted to test hypotheses derived from those models. This review clearly shows that the interaction between theoretical and empirical studies has facilitated understanding of the evolutionary conditions of diverse sexual strategies among crustaceans. Since sexual strategies often interact with other aspects of adaptive strategies such as life history, integrating different aspects into both theoretical and empirical studies will provide further understandings into crustacean sexual systems. In addition, the authors point out the potential of phylogenetic comparative analyses using natural history data as a tool to understand the tempo and mode of evolution of sex allocation strategies.

Crustacean Reproductive Records

Crustacean reproductive traits are highly diverse, and this chapter illustrates some of the most extreme cases, placing them in the context of the more typical crustaceans. It highlights, for example, the male and female records of size and age, the “hottest” and “coolest” reproducers, the longest penises, the largest sperm and eggs, the smallest and largest brood sizes, the longest mate guarding, the most massive sexually selected weapons, the flashiest courtship, the most fathers per brood, the longest incubation of broods, the smallest and largest larvae, the longest larval duration, the longest dormancy of eggs, and the oldest fossil evidence of penis, sperm, brood care, and larvae. Using these illustrious case studies, this chapter briefly examines the adaptive advantages of these extremes and discusses why few species have evolved unusual reproductive traits. Crustaceans indeed appear to hold animal records with respect to relative penis length, aflagellate sperm length, dormant egg viability and fossil ages of penis, giant sperm, and brood care. These captivating examples may be of applied importance in terms of restoring human-altered ecosystems (resurrection ecology using egg banks) and in management strategies of important fisheries.

“The Caring Crustacean”: An Overview of Crustacean Parental Care

Many crustacean species are known to provide parental care, with behaviors ranging from ventilating the eggs to providing food for young. This chapter provides an overview of parental care patterns across crustaceans, and then compares crustacean parental care to that of select other taxa (insects, fishes, frogs) that share important traits with crustaceans (exoskeleton, aquatic or amphibious lifestyle, respectively). The aim is to identify gaps in the understanding of the evolution of parental care in crustaceans. We show that nearly all crustaceans provide parental care for early embryos (eggs), while caring for advanced stages is rarer. The most common forms of care are simple behaviors (e.g. fanning and cleaning behaviors), while complex behaviors (e.g. feeding the young) evolved exclusively in groups that also care for longer. Caring is most frequently done by females, while biparental is rare, and exclusive paternal care is nonexistent. When compared across taxa, simple behaviors are also the most common forms of care, and reasons for the evolution of parental care have common themes. First, parental care enhances offspring survival. In crustaceans, early embryo/egg mortality is apparently high, which might have triggered the evolution of parental care in several crustacean taxa independently. Second, crustaceans that have large eggs and inhabit stable habitats tend to care for longer. Lastly, internal fertilization seems to prevent male crustaceans from caring by not allowing the males to access the eggs and to ensure paternity.