Sexual Signals Persist over Deep Time: Ancient Co-option of Bioluminescence for Courtship Displays in Cypridinid Ostracods

Abstract

Although the diversity, beauty, and intricacy of sexually selected courtship displays command the attention of evolutionists, the longevity of these traits in deep time is poorly understood. Population-based theory suggests sexual selection could either lower or raise extinction risk, resulting in high or low persistence of lineages with sexually selected traits. Furthermore, empirical studies that directly estimate the longevity of sexually selected traits are uncommon. Sexually selected signals-including bioluminescent courtship-originated multiple times during evolution, allowing the empirical study of their longevity after careful phylogenetic and divergence time analyses. Here, we estimate the first transcriptome-based molecular phylogeny and divergence times of Cypridinidae. We report extreme longevity of bioluminescent courtship, a trait important in mate choice and probably under sexual selection. Our relaxed-clock estimates of divergence times coupled with stochastic character mapping show luminous courtship evolved only once in Cypridinidae-in a Sub-Tribe, we name Luxorina-at least 151 millions of years ago from cypridinid ancestors that used bioluminescence only in antipredator displays, defining a Tribe we name Luminini. This time-calibrated molecular phylogeny of cypridinids will serve as a foundation for integrative and comparative studies on the biochemistry, molecular evolution, courtship, diversification, and ecology of cypridinid bioluminescence. The persistence of luminous courtship for hundreds of millions of years suggests that sexual selection did not cause a rapid loss of associated traits, and that rates of speciation within the group exceeded extinction risk, which may contribute to the persistence of a diverse clade of signaling species. [Ancestral state reconstruction; Biodiversity; co-option; divergence time estimates; macroevolution; Ostracoda; phylogenomics; sexual selection.].

Figure 1.

Species phylogeny inferred using multispecies-coalescent and transcriptome data. Circles at nodes indicate 1.0 posterior probability, and nodes with values less than 1.0 are indicated numerically. Circles at tips represent nonluminous (lightest), luminous but noncourtship signaling (medium shade), and species with luminous courtship (darkest shade). The three described genera of signaling species are labeled at the top, along with “Z-group,” which is a clade of signaling species plus Vargula tsujii. Vargula is polytypic (see also Cohen and Morin 2003; Morin 2019) and the type species is outside this group, so formally, these should not be Vargula. Above the tree, we also labeled noncypridinid Outgroups and Cypridinidinae. We herein suggest a name for the bioluminescent Cypridinidae to be Tribe Luminini (for lumen light and the typical Tribe suffix for zoology) and a name for the clade containing courtship signaling cypridinids to be Sub-Tribe Luxorina (lux light uxoriae courtship -ina typical zoological subtribe suffix). Locality abbreviations for collecting sites of species are above each tip as follows: AU Australia, BZ Belize, CA California, USA, CU Curacao, JA Jamaica, JP Japan, PA Panama, PP Previously Published, PR Puerto Rico, and RO Roatan, Honduras (see Supplementary Table S1 available on Dryad for specific localities). Above locality names are abbreviations for species. Described species are abbreviated as the first letter of genus and first three letters of species epithet; undescribed species outside of Luxorina are labeled as the first three letters of genus followed by sp. or two locality or collector letters when there are more than one undescribed species from the genus; within Luxorina, we used 2–4 letter field codes for undescribed species (see Supplementary material available on Dryad for tree with full species names).

Figure 2.

Expanded taxon sampling by adding individual mitochondrial genes, mainly from Torres and Gonzalez (2007) to the transcriptome data in Figure 1. We inferred this species phylogeny using the multispecies coalescent. Taxa colored pink (light grey) are those that contain only mitochondrial data. Small colored circles at nodes indicate posterior probabilities low (0.330.59) black, medium (0.600.76) yellow (lightest shade), high (0.951.0) red (medium shade). Locality abbreviations are as in Figure 1 and also include additional locations of VI US Virgin Islands and FL Florida USA. For Jimmorinia (*), we combined data from transcriptomes from a Jamaican species (J. cf gunnari) with mitochondrial DNA from a specimen (Jimmorinia sp. USVI) unidentified to species from VI. Pie charts represent proportions of likelihood values for alternative ancestral states. Bioluminescence was most likely absent (white) prior to Luminini, as supported by a significantly high proportion of likelihood for the absence of bioluminescence compared to the presence (medium shade). Significantly high likelihood proportions first appear in Luminini for bioluminescence (medium shade) and Luxorina for bioluminescent courtship signaling (darkest shade), compared to the absence of those traits (black), which were analyzed separately as binary traits (see Supplementary material available on Dryad for full ancestral state reconstruction results).

Figure 3.

Time of taxon origins based on relaxed molecular clock analysis. a) We used two fossil constraints (green circles): Myodocopida, with offset exponential prior with a minimum of 448.8 Ma and maximum of 509 Ma and Ostracoda with a uniform prior between 443.8 and 509 Ma (Oakley et al. 2013; Wolfe et al. 2016) to estimate divergence times across our phylogeny; b) Results of time-tree stochastic character mapping (ttscm) estimates origin of bioluminescence to be 267 Ma because that is the median age of character state transitions to bioluminescence; c) Similarly, ttscm estimates the origin of luminous courtship to be 213 Ma.