Pipefish and Seahorse Research

Lined Seahorse
(photo by Mary Wicksten)

Male Pregnancy and Sexual Selection

Male pregnancy is ubiquitous in the fish family Syngnathidae, which includes pipefishes, seahorses and sea dragons. During mating, the female transfers unfertilized eggs to the ventral surface of the male, where they are fertilized by the male's sperm. In some species, the eggs are simply attached to the surface of the male, while in other species they are covered by a fleshy pouch.

Beyond being a curiosity, male pregnancy is of interest to evolutionary biologists because it affects the nature of sexual selection. In most biological systems, males compete with one another for mating opportunities, and secondary sex traits (like antlers in deer or striking plumage in birds) typically evolve in males. In some species of pipefish, however, females compete for access to receptive males and the secondary sex traits evolve in females. This reversal in the direction of sexual selection provides an interesting challenge for theories of sexual selection. Thus, we have been interested in the study of mating patterns and sexual selection in these interesting fishes.

Egg Competition and Cryptic Male Choice in Pipefish

One major goal of the Jones lab is to understand the post-copulatory processes that are important to sexual selection. One such process is gamete competition or choice. In a NSF-funded project, we are collaborating with Ingrid Ahnesjö, Anders Berglund, Charlotta Kvarnemo, and Gunilla Rosenqvist to study post-copulatory selection in Syngnathus typhle. We already know that brood reduction is a common phenomenon in this species. Males usually give birth to far fewer offspring than the number of eggs they initially receive during mating. We also know that most males receive eggs from multiple females during a single pregnancy. We do not know whether brood reduction is adaptive. We also do not know to what extent a particular offspring's chance of survival within the pouch is due to male versus female effects. We are currently wrapping up several projects that will resolve some of these questions.

The Initial Gulf Pipefish Microarray Test Chip
(produced by A. Harlin-Cognato in T. Thomas' LFG)

Genetics and Genomics of Male Pregnancy in Pipefishes and Seahorses

We are interested in morphological evolution, and one important step in the evolution of morphology is the genesis of novel structures. Thus, we are pursuing a deeper understanding of the steps involved in the evolution of male pregnancy, with a particular emphasis on the male's specialized pregnancy structure, the brood pouch. Initially, we have been identifying genes involved in male pregnancy, which by definition have been co-opted for a new role in the brood pouch, and looking at the molecular evolution of these genes. Two important questions are whether or not gene duplication and positive selection accompany co-option events. Eventually, we would like to understand the development of the brood pouch structure.

The brood pouch is of particular interest, because it represents a case of parallel evolution. The family Syngnathidae is divided into two groups that diverged early during the diversification of the group. Males from one group carry the eggs on their abdomens, whereas males of the other group carry the eggs on their tales. The actual brood pouch evolved independently in these two groups, so we would like to know whether or not the same evolutionary events accompanied the evolution of this structure in these distinct lineages.

Our research in this area involves a number of techniques, including cDNA libraries, quantitative real-time RT-PCR, DNA sequencing, and a cDNA microarray that is under construction for the Gulf pipefish. Current members of the Jones Lab are collaborating with April Harlin-Cognato on various topics in brood pouch evolution.

Comparative Studies of Mating Systems in Seahorses and Pipefishes

In addition to the seahorse studies, we have conducted molecular studies on several species of pipefish. The mating systems range from the monogamous mating system of seahorses to polygynandry (both sexes mate multiply) and extreme polyandry (females mate multiply but males mate once). In general, the polyandrous species (Syngnathus scovelli and Nerophis ophidion) appear to experience a greater intensity of sexual selection and are more sexually dimorphic than the monogamous (H. subelongatus) and polygynandrous species (S. floridae and S. typhle).

Jones, A. G. and J. C. Avise. 1997. Microsatellite analysis of maternity and the mating system in the Gulf pipefish (Syngnathus scovelli), a species with male pregnancy and sex-role reversal. Molecular Ecology 6:203-213.

Jones, A. G. and J. C. Avise. 1997. Polygynandry in the dusky pipefish Syngnathus floridae revealed by microsatellite DNA markers. Evolution 51:1611-1622.

Jones, A. G., G. Rosenqvist, A. Berglund, and J. C. Avise. 1999. The genetic mating system of a sex-role-reversed pipefish (Syngnathus typhle): a molecular inquiry. Behavioral Ecology and Sociobiology 46:357-365.

Jones, A. G., D. Walker, and J. C. Avise. 2001. Genetic evidence for extreme polyandry and extraordinary sex-role reversal in a pipefish. Proceedings of the Royal Society of London B: Biological Sciences 268:2531-2535.

Jones, A. G. and J. C. Avise. 2001. Mating systems and sexual selection in male-pregnant pipefishes and seahorses: insights from microsatellite-based studies of maternity. Journal of Heredity 92:150-158.

McCoy, E. E., A. G. Jones, and J. C. Avise. 2001. The genetic mating system and tests for cuckoldry in a pipefish species in which males fertilize eggs and brood offspring externally. Molecular Ecology 10:1793-1800.

Broad-nosed Pipefish
(photo by A. Berglund)

Experimental Studies of Pipefish Mating Patterns

In collaboration with Anders Berglund and Gunilla Rosenqvist, we couple breeding experiments in the laboratory with molecular analyses to study sexual selection. These studies have led to insights about how sexual selection should be measured in natural populations (see also the Parentage Analysis link) and how mate quality affects male mating patterns.

Jones, A. G., G. Rosenqvist, A. Berglund, S. J. Arnold, and J. C. Avise. 2000. The Bateman gradient and the cause of sexual selection in a sex-role-reversed pipefish. Proceedings of the Royal Society of London B: Biological Sciences 267:677-680.

Jones, A. G., G. Rosenqvist, A. Berglund, and J. C. Avise. 2000. Mate quality influences multiple maternity in the sex-role-reversed pipefish Syngnathus typhle. Oikos 90:321-326.

Jones, A. G., G. Rosenqvist, A. Berglund, and J. C. Avise.  2005.  The measurement of sexual selection using Bateman’s principles: an experimental test in the sex-role-reversed pipefish Syngnathus typhle.  Integrative and Comparative Biology 45:874-884.

Monogamy in Seahorses (genus Hippocampus)

Our molecular studies of parentage have verified that one species of seahorse, H. subelongatus (formerly H. angustus), is genetically monogamous and that pair bonds usually persist over multiple pregnancies within a breeding season. No one has yet been able to follow the mating patterns of individual seahorses in different seasons, so we do not know if their pair bonds persist for multiple years. See the following papers for more details:

Jones, A. G., C. Kvarnemo, G. I. Moore, L. W. Simmons, and J. C. Avise. 1998. Microsatellite evidence for monogamy and sex-biased recombination in the Western Australian seahorse, Hippocampus angustus. Molecular Ecology 7:1497-1505.

Kvarnemo, C., G. I. Moore, A. G. Jones, W. S. Nelson, and J. C. Avise. 2000. Monogamous pair bonds and mate switching in the Western Australian seahorse Hippocampus subelongatus. Journal of Evolutionary Biology 13:882-888.

One important question is whether or not geographic or temporal variation in mating systems is an important factor in the evolution of mating patterns in these species. This topic has addressed very sparingly in the mating system literature in general. Kenyon Mobley will study this issue as part of his doctoral dissertation.

Sympatric Speciation in Seahorses

Our recent research on mating patterns in seahorses indicates that they mate assortatively by size and that the strength of assortative mating may be sufficient to promote sympatric speciation. Phylogenetic and biogeographic data support this idea. Future research will be needed to establish exactly how important assortative mating has been to the evolutionary legacy of seahorses and pipefishes. We intend to pursue this interesting topic in future studies.

Jones, A. G., G. I. Moore, C. Kvarnemo, D. Walker, and J. C. Avise. 2003. Sympatric speciation as a consequence of male pregnancy in seahorses. Proceedings of the National Academy of Sciences USA 100:6598-6603.